Abstract

Background:Spinal arteriovenous fistulae (AVF) located at the craniocervical junction (CCJ) are rare and usually present with hemorrhage. Bleeding is usually attributed to arterial feeders arising from the anterior spinal artery (ASA) and aneurysms located on such feeders. Perimedullary AVFs are typically found on the ventral surface of the spinal cord, which makes them difficult to treat through traditional microsurgical methods. In addition, their unique vessel angioarchitecture frequently precludes safe embolization. We present the first case of a CCJ perimedullary AVF successfully treated using flow diversion.

Case Description:A 76-year-old man was brought to the emergency department after suddenly losing consciousness. On further evaluation, infratentorial subarachnoid hemorrhage and a perimedullary AVF at the ventral surface of the spinal cord were identified. The ASA originated from the left V4 segment, providing a single feeder to the lesion associated with a 2 mm aneurysm. After initial antiplatelet loading, 8 hydrophilic polymer-coated flow diverters were deployed to cover the ASA’s origin in two sessions, achieving the complete occlusion of the lesion and the aneurysm 5 months later, without evidence of ischemic lesions.

Conclusion:CCJ perimedullary AVFs can bleed with devastating consequences. These lesions can be challenging to treat through traditional microsurgical or endovascular techniques. Progressive occlusion with flow diversion is feasible in single-feeder AVFs, theoretically allowing blood flow reorganization to the cervical spinal cord.

Keywords: Craniocervical junction, Flow diversion, Perimedullary arteriovenous fistula

INTRODUCTION

Dural arteriovenous fistulas (AVFs) found at the craniocervical junction (CCJ) are rare, accounting for <2% of all spinal AVFs.[ 2 , 10 ] These lesions exhibit unique clinical features, angioarchitecture, and outcomes compared to fistulas located in other regions. For example, CCJ AVFs typically cause acute neurological deficits, mainly due to subarachnoid or intramedullary hemorrhage, in contrast to thoracolumbar lesions that usually present with venous congestion.[ 2 , 12 , 17 ] When bleeding occurs, it is generally attributed to the rupture of a flow-related aneurysm located on one of the fistula’s arterial feeders;[ 3 ] therefore, digital subtraction angiography (DSA) becomes essential in determining their complex angioarchitecture and potential weak points. Given their low prevalence, the treatment is usually determined on a case-by-case basis by a multidisciplinary team of neurosurgeons and interventional neuroradiologists. This has led to a range of different treatment methods being recommended primarily based on case reports or small case series. These methods include conservative therapy, surgery, transvenous and transarterial embolization, electrocoagulation, or combined approaches.[ 3 , 6 , 11 , 12 , 16 ] This manuscript presents the first reported case of a ruptured CCJ perimedullary AVF successfully treated with multiple flow diverters (FDs) deployed in the parent vessel of the respective pial feeding artery and the rationale behind this approach.

CLINICAL PRESENTATION

History and examination

A 76-year-old man with a previously known gait disorder was brought to the emergency department after suddenly losing consciousness. On arrival, the Glasgow coma scale score was 3, although brainstem reflexes were still present. The patient was thus intubated, and an initial head computed tomography (CT) scan revealed the presence of infratentorial acute subarachnoid hemorrhage (SAH) (Hunt-Hess grade V and modified Fisher Scale grade 4). In addition, a 6 mm vascular structure was identified on CT angiography at the ventral pial surface of the spinal cord located at the CCJ level, suggestive of an anterior spinal artery (ASA) aneurysm [ Figures 1a - c ]. A subsequent DSA revealed the presence of a perimedullary AVF on the ventral spinal cord surface at the level of the foramen magnum. The analysis of the lesion’s angioarchitecture determined that the ASA originated exclusively from the V4 segment of the left vertebral artery (VA). A single pial AVF feeder originated from the ASA, which had a 2 mm aneurysmal dilation, later considered the most probable source of bleeding. In addition, the AVF drained through a radiculopial vein along the right-sided C1 nerve root to the epidural venous plexus, with no other radiculomedullary ASA feeders or arteriovenous (AV) shunts seen at the craniocervical and cervical levels [ Figures 1d - h ]. After identifying the potential bleeding source of the lesion, treatment was considered necessary. Consequently, informed consent was obtained from the patient’s family.

Figure 1:

A 76-year-old patient with a ruptured craniocervical junction (CCJ) perimedullary arteriovenous fistulae (AVF). (a) An axial non-contrast CT scan showed infratentorial subarachnoid hemorrhage (SAH) classified as Hunt-Hess grade V and modified Fisher Scale grade 4. CT angiography, (b) sagittal, and (c) coronal views, identified an abnormal vascular structure at the ventral surface of the spinal cord, suggestive of an anterior spinal artery (ASA) aneurysm (white arrows). Digital subtraction angiography (DSA), (d) a posteroanterior (PA) right vertebral artery (VA) injection showed no contribution to the ASA or the lesion. Left VA injection, (e) PA early arterial and (f) late arterial phases; right anterior oblique projection, (g) early and late (h) arterial phases. A perimedullary AVF was identified draining through a radiculopial vein along the right C1 nerve root to the epidural venous plexus (white asterisk). The ASA originated from the left V4 segment (white arrowheads) and supplied a small AVF feeder that had a 2 mm aneurysm (white arrows).

Treatment

The ASA’s small diameter and anterograde filling [ Figure 2a ] precluded any attempt to perform a safe transarterial liquid embolization or coiling procedure without risking spinal cord infarction. Moreover, the ventral location of the shunt and aneurysm made any open microsurgical procedure a technically challenging alternative, and the postoperative prognosis was considered unfavorable.[ 5 ] Thus, a novel approach was considered to induce gradual reduction of afferent blood flow to the lesion through flow diversion, and thus, antiplatelet treatment consisting of aspirin (1000 mg IV), ticagrelor (180 mg through the nasogastric tube), and eptifibatide (IV bolus; bodyweight adapted) was administered. A 0.021” microcatheter (Rebar 18; Medtronic; Dublin, Ireland) was used to deploy 6 overlapped non-matching FDs (1 × p64 MW HPC 3/9 mm, 3 × p48 MW HPC 3/9 mm, and 2 × p48 MW HPC 2/12 mm; WallabyPhenox; Bochum, Germany) in the left V4 segment, thus creating a dense coverage at the ASA’s origin [ Figure 2b ], similar to a previously documented institutional experience treating other high-flow shunts.[ 15 ] Immediately after FD deployment, there were no relevant angiographic changes [ Figures 2c and d]. Dual antiplatelet therapy (aspirin 500 mg IV b.i.d. and ticagrelor 90 mg PO b.i.d.) was continued and monitored with the Multiplate (Roche; Basel, Switzerland) and VerifyNow (Accumetrics, San Diego, USA) assays. No signs of postprocedural ischemic lesions were discovered on diffusion-weighted imaging [ Figure 2e ]. A tracheostomy was performed on Day 7, and after sedation was suspended, the patient was awake, disoriented, and was able to partially move all extremities symmetrically. A follow-up DSA on Day 11 showed significantly reduced blood flow to both lesions and [ Figure 2f ] 2 additional FDs (2 × p48 MW HPC 2/15 mm) were successfully implanted, overlapping the prior construct. The patient was discharged to rehabilitation on Day 21, and after 5 months, angiographic follow-up showed complete occlusion of the AVF and aneurysm [ Figure 2g ], while magnetic resonance imaging (MRI) showed no signal abnormalities of the brain stem or cervical spinal cord suggesting ischemia or lesion remnants [ Figure 2h ]. The patient’s condition gradually improved, and he returned to his baseline status before the bleeding episode, including the pre-existing gait disturbance (modified Ranking scale 1).

Figure 2:

Endovascular treatment and follow-up. First session, left anterior oblique left vertebral artery (VA) injection, (a) before treatment and after 6 hydrophilic polymer-coated flow diverters (FDs) were deployed: (b) unsubtracted, (c) subtracted, and (d) 3D rendering views of the V4 segment. The procedure was uneventful, and the anterior spinal artery (ASA) remained patent after treatment (white arrowheads). (e) No signs of ischemic lesions after the procedure were noted on diffusion-weighted imaging. (f) After 11 days, left VA injection showed a still patent ASA (white arrowheads) with reduced opacification of the aneurysm (white arrow) and arteriovenous fistula. Two additional FDs were implanted, (g) and after 5 months, ASA anterograde filling was no longer observable, and no evidence of the aneurysm and fistula remained. (h) Craniocervical T2-weighted imaging, sagittal view. There was no radiological evidence of myelopathic changes or the lesion in the cervical spinal cord, which correlated with the patient’s favorable neurological recovery.

DISCUSSION

Although rare, CCJ spinal AVFs are associated with a significantly higher chance of bleeding.[ 14 ] In a case series of 38 patients, Zhong et al. reported that 95% of cases presented with SAH at the moment of diagnosis. Superolateral venous drainage was significantly associated with hemorrhagic presentation, unlike caudal drainage, which was often associated with myelopathy.[ 17 ] Moreover, a multicenter study found that 73% of cases presented with bleeding, and this type of presentation was related to ASA feeders, feeder-located aneurysms, and radicular-type AVFs.[ 3 ] Nevertheless, the natural history of these lesions is still largely unknown, but, given that our patient displayed some of these features, a multidisciplinary evaluation concluded that treatment could lower the potential risk of a second hemorrhagic episode.

The CCJ is a complex region that presents several challenges for both open and endovascular approaches. A tailored occipital craniotomy with C1 hemilaminectomy assisted by intraoperative angiography is usually the preferred treatment strategy due to its high rate of complete AVF occlusion.[ 4 , 13 , 17 ] However, perimedullary AVFs, in particular, are often found on the ventral surface of the spinal cord, which complicates the identification and control of their arterial feeders using traditional microsurgical techniques.[ 4 ] Arterial feeders at this level arise from the VA at a straight angle, follow a tortuous trajectory, and have a small caliber, all features associated with risks of incomplete occlusion or iatrogenic vessel perforation during transarterial embolization.[ 7 ] On the other hand, transvenous embolization has been proposed as an alternative, although it is seldom attempted since it requires accessible veins,[ 16 ] which were unavailable in this case.

A similar concept has been demonstrated with the use of FDs to treat direct carotid-cavernous sinus fistulae. Although this is still considered an off-label use with the exception of the p64 FD in Europe, favorable results have been obtained in selected cases. Importantly, achieving progressive occlusion of the fistula may require multiple layers of FDs,[ 8 ] in contrast to aneurysm treatment, and may take weeks to months depending on the shunt’s blood flow level.[ 15 ] A similar phenomenon was observed in a traumatic vertebral-venous fistula case report also treated with flow diversion.[ 9 ] The feasibility and safety of this concept is further demonstrated by our case, where despite the lack of pial supply to the ASA from the contralateral VA and the loss of ipsilateral pial supply during follow-up, a favorable angiographic and clinical outcome was achieved without evidence of ischemia or myelopathic changes affecting the cervical spinal cord [ Figures 2e and h ]. Similarly, a multicenter study found no cases of spinal cord infarction after flow diversion treatment for posterior circulation aneurysms despite that, in 3 patients, a covered ASA ended up occluding during follow-up.[ 1 ] Regardless, the theoretical risk of spinal cord infarction remains, making this approach feasible solely in exceptional circumstances when surgery and direct endovascular embolization are deemed unsuitable.

Limitations

The objective of this manuscript was to illustrate a potential alternative for treating these rare and challenging lesions, particularly when other techniques are considered unsuitable. However, the cost of therapy can significantly increase when multiple FDs are used, and there may be a greater risk of rebleeding due to the need for intense platelet inhibition during the latency period required for occlusion. More cases with longer follow-up periods are needed to validate this concept.

CONCLUSION

To our knowledge, this is the first report of a ruptured CCJ perimedullary AVF successfully treated with FD. This treatment modality could constitute a surgical alternative for single-feeder, ventrally located lesions.

Ethical approval

The Institutional Review Board has waived the ethical approval for this study.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship

Nil.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

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