Adjunctive venous sinus stenting in transvenous embolization of vein of Galen malformations

Abstract

Background

Vein of Galen malformations are congenital arteriovenous malformations primarily treated by endovascular embolization via transarterial or transvenous approaches. transvenous embolization can be utilized to close the malformation but may be difficult in patients with venous stenosis or blockages, which drive venous hypertension and lead to significant neurologic consequences. Here, we illustrate the atypical placement of an intracranial venous sinus stent to improve outflow after transvenous embolization in pediatric patients with the vein of Galen malformation.

Methods

A retrospective review of clinical databases at two high-volume endovascular centers from January 2018 to March 2023 identified all vein of Galen malformation patients who received a venous sinus stent during transvenous embolization. Clinical data, imaging, angioarchitecture, operative details, postoperative management, and follow-up were reviewed.

Results

Three patients presented for transvenous embolization after multiple staged transarterial embolizations of their vein of Galen malformation. Transvenous access was complicated by lateral sinus stenosis, which was temporarily relieved by balloon angioplasty. After transvenous embolization by pressure cooker technique, the dural sinuses were stented using the existing venous guide catheter. Venous angiography demonstrated improved flow across the stenosed areas and post-embolization angiography demonstrated normalized venous drainage with widely patent stents. One patient experienced postoperative oculomotor nerve palsy unrelated to the stent placement. All patients demonstrated a complete cure of their vein of Galen malformations with patent venous sinus stents on follow-up.

Conclusion

In patients with the vein of Galen malformation and venous hypertension receiving transvenous embolization, venous sinus stenting may be a safe and effective option to reduce aberrant cortical venous drainage and improve normal outflow. Further studies are warranted to investigate its benefit in high-flow vascular malformations.

Introduction

Vein of Galen malformations (VOGMs) are congenital arteriovenous malformations (AVM) connecting the choroidal circulation to a persistent median prosencephalic vein of Markowski, the embryonic precursor to the vein of Galen.^1,2 Neonates who are symptomatic typically have more severe presentations with signs of early high-output heart failure and an increased risk of morbidity and mortality. ³ Infants, on the other hand, typically present with hydrocephalus, seizures, and developmental delays.^3,4 VOGM are typically managed by endovascular embolization, through either a transarterial or transvenous approach. ⁴ The decision to utilize each of these approaches involves multiple considerations. Staged transarterial embolization (TAE) is generally safe and considered to be the gold standard for treating VOGM. ⁵ However, as the malformation is repeatedly embolized, arterial access becomes more challenging due to the progressively reduced size of the available feeders for catheterization. Obtaining complete closure of the VOGM is ideal to avoid long-term sequelae. In cases where the remaining arterial feeders are limited to small thalamoperforators or other vessels, transvenous embolization (TVE) provides an attractive alternative for obtaining complete closure of the malformation. ⁶ TVE offers the benefit of a higher rate of closure. However, TVE is inherently riskier: the risks of venous congestion and hemodynamic remodeling, venous sinus outflow restriction with associated hyperemia and cerebral edema, subsequent hemorrhage, and neurologic deficits are noticeably higher in TVE. TVE as an approach has a higher mortality rate. ⁷ Though transvenous approaches to embolizing VOGM are successful, especially with the advent of newer techniques such as the pressure cooker technique, more progress needs to be made to further increase the safety of TVE.^8–10 TVE can also be limited in patients with VOGM due to poor access, as a notable subpopulation of patients develop comorbid dural venous sinus stenosis which prevents the passage of a guidewire or microcatheter. ¹¹ These patients often present with more severe and refractory symptoms, leading to persistent long-term neurologic deterioration and a higher risk of morbidity and mortality during embolization procedures.

Intracranial venous sinus stenting (VSS) has gained popularity as a method to relieve venous sinus stenosis, both primary stenosis and stenosis secondary to intracranial pathologies such as tumors, venous sinus thrombosis, and more. ¹² In adults and in children, VSS has been utilized in the symptomatic management of idiopathic intracranial hypertension and pulsatile tinnitus secondary to lateral sinus stenosis.^13,14 VSS has been demonstrated to restore normal flow through stenotic sinuses without a high rate of complication. Patients at high risk of outflow restriction due to underlying stenosis or poor drainage may benefit from adjunctive VSS to improve normal drainage through the venous sinuses. Here, we present three cases with atypical uses of intracranial venous sinus stenting to relieve outflow restriction after TVE of a VOGM and discuss the technical aspects of its use.

Methods

This study was approved by the Institutional Review Board (IRB) at the senior author's institution. Clinical data, operative records, and imaging from July 2019 to March 2024 were retrospectively obtained from the database of two high-volume endovascular centers and reviewed. All VOGM patients who received an intracranial venous sinus stent were reviewed.

All procedures were performed under general anesthesia. Right femoral arterial access was obtained using ultrasound guidance, and a 5F Glidesheath Slender (Terumo, Tokyo, Japan) was placed and maintained on a heparinized saline flash line. A 5F Envoy guide catheter (Cerenovus, Irvine, CA, USA) was then advanced into the aortic arch and six-vessel diagnostic cerebral angiography was performed by selective catheterization with roadmapping, digital fluoroscopy, and careful guidewire manipulation.

The right jugular vein was accessed by a combination of ultrasound navigation and angiographic road mapping. A 4Fr sheath was advanced over a microguidewire and venous angiographic runs confirmed access catheter positioning within the right jugular vein. This access was dilated until an 8Fr short sheath could be passed into the jugular vein. When the 8Fr guiding catheter was unable to pass the stenosed dural venous sinus, balloon angioplasty was performed using a Sterling balloon dilatation catheter (Boston Scientific, Marlborough, MA, USA) to temporarily reopen the sinus and pass the area of stenosis with the guiding catheter. The guiding catheter was then navigated to the straight or falcine sinus and transvenous embolization was performed by pressure cooker technique, as demonstrated previously by Chapot et al. ⁸ and Shigematsu et al. ¹⁰ After successful embolization, the venous anatomy was assessed for residual stenosis. A Carotid Wallstent (Boston Scientific, Marlborough, MA, USA) was delivered to the dural venous sinus over the existing guidewire and deployed across the stenosed area. If necessary, a second balloon angioplasty was performed using another Sterling balloon catheter to aid post-stent dilatation. Placement of the stent was confirmed with venous angiography and flow was assessed using control angiographic runs.

Illustrative cases

Case 1

An ex-39-week female newborn delivered by normal spontaneous vaginal delivery was found to have a VOGM on head ultrasound during workup for a cardiac murmur and right ventricular hypertrophy. The baby was managed medically, but was eventually transferred to the senior author's institution and received her first neonatal embolization. She subsequently received nine staged TAEs over 3 years with progressive improvement in her symptoms and cognitive delay as flow through the malformation decreased. After the ninth TAE, transarterial approaches to the malformation were now complicated and the remaining small-caliber feeders were difficult to catheterize. Due to the progressive reductions of the venous component and current arterial morphology preventing uncomplicated transarterial access, she was now considered to be a good candidate for a transvenous approach to close the malformation. At the time of the procedure, she was doing well. She received physical therapy (PT), occupational therapy (OT), and speech therapy 5 times per week for residual left-sided weakness and global developmental delay.

Subtracted angiography of the left vertebral artery (LVA) prior to the transvenous approach demonstrated the known VOGM with venous hypertension supplied by distal branches of thalamoperforators and bilateral posterior cerebral arteries (Figure 1A and B). An area of stenosis at the right sigmoid-jugular junction was present. Due to this stenosis, the 8Fr guide catheter could not be passed and so a balloon angioplasty was performed to relieve the stenosis (Figure 1C). Subsequent angiography demonstrated improved vessel diameter and the guide catheter was able to access the straight sinus. TVE was performed using the Chapot pressure cooker technique, after which shunting was significantly reduced but still present from the thalamoperforators. The underlying stenosis at the right sigmoid-jugular junction was still present, and so due to concern about restenosis of the area, the decision was made to proceed with VSS. A 6 × 22 mm Carotid Wallstent was deployed across the stenosed area from the right sigmoid sinus to the internal jugular vein and another balloon angioplasty was performed (Figure 1D). Subsequent control angiography showed significantly reduced shunting, with the majority of the blood draining into the right transverse-sigmoid sinuses and with improved venous diameter and flow across the stented junction.

Figure 1.

Subtracted AP (A) and lateral (B) views of the left vertebral artery demonstrate a VOGM with venous hypertension supplied by distal branches of thalamoperforators and bilateral posterior cerebral arteries. The left sigmoid sinus was not opacified and the left transverse sinus was draining into a dominant cerebellar cortical vein to a spinal vein as well as a dominant vein of Labbe into the sylvian vein into the cavernous sinus. An area of stenosis at the right sigmoid-jugular junction (circle) was present. (C) AP X-rays demonstrate the inflation of a balloon across the stenosed right sigmoid-jugular junction. (D) AP venous angiography demonstrates improved flow across the stenosed area after placement of the venous sinus stent (arrow). (E) Subtracted lateral views of the left vertebral artery after a second transvenous embolization demonstrate persistent complete obliteration of the VOGM with patent stents. The majority of the flow continues to drain through the stented right sigmoid sinus.

AP: angioplasty; VOGM: vein of Galen malformation.

Postoperatively, the patient was started on aspirin 81 mg daily for the new stent and stayed in the PICU for 4 days. They were maintained on their regular dose of levetiracetam and received strict blood pressure control with frequent neurological checks. A subsequent clinical follow-up demonstrated improvement in milestones, and the patient eventually received a second TVE through the stent which resulted in a stable cure of their VOGM seen on six-month follow-up (Figure 1E). Clinical follow-up 3 months after cure demonstrated a patent stent on imaging. The patient progressed in their milestones to a developmental stage typical for a child of their age, with reduced need for PT, OT, and speech therapy.

Case 2

A one-week-old male newborn presented with hydrocephalus and signs of heart failure after a VOGM was diagnosed in utero. Subtracted cerebral angiography of the left internal carotid artery during embolization demonstrated a dilated Vein of Galen varix with venous hypertension. The patient underwent two staged TAEs over the next year of life and was then considered eligible for TVE at 15 months of age. Subtracted angiography prior to embolization redemonstrated the dilated VOGM with a high degree of shunting. Both sigmoid sinuses were not opacified, the right transverse sinus was draining into a dominant cortical cerebellar vein, and the left transverse sinus was draining into a dominant Vein of Labbe (Figure 2A). Stenosis was noted at the right sigmoid-jugular junction.

Figure 2.

(A) Subtracted AP angiogram of the left vertebral artery in the venous phase demonstrates the VOGM with venous hypertension. Neither sigmoid sinus is opacified: the right transverse sinus drains to a cortical cerebellar vein while the left transverse sinus drains to a dominant vein of Labbe. (B) After angiography with stent placement, improved flow is seen through the right sigmoid-jugular junction. (C) Axial T1-weighted MRI with contrast on 2-year follow-up demonstrates the patent stented right internal jugular vein (arrow).

VOGM: vein of Galen malformation; MRI: magnetic resonance imaging; AP: angioplasty.

Due to stenosis, the guide catheter could not be passed and so a balloon angioplasty was performed to relieve the stenosis. After the improvement in the vessel diameter, TVE was performed using the Chapot pressure cooker technique. To protect against possible restenosis, a venous sinus stent was then placed within the right sigmoid-jugular junction, from the right sigmoid sinus to the internal jugular vein, to ensure appropriate venous drainage. With the stent in place, normal opacification of the bilateral sinuses was achieved. Control angiography through the right vertebral artery after placement of the stent demonstrated improved and normalized flow through the malformation (Figure 2B). Both sinuses were now opacifying.

Postoperatively, the patient was started on 81 mg aspirin daily and had an uneventful stay in the PICU. Subsequent clinical follow-up demonstrated notable neurologic improvements, and radiographic follow-up 2 years later demonstrated a patent stent on MRI without complication (Figure 2C).

Case 3

A 7-year-old boy diagnosed with a VOGM at 2 weeks of age, managed with a ventriculo-peritoneal shunt at 5 months of age which was revised at 2 years of age at another hospital, presented to our practice with cognitive delays and oculomotor symptoms. He was scheduled for angiography and first-stage embolization. He underwent four staged TAEs over 7 years, achieving near-total obliteration of the malformation, and was considered amenable for a curative TVE. At the time of his TVE, he was asymptomatic. Subtracted angiography prior to the embolization demonstrated the VOGM after multiple embolizations with slow emptying into a hypertrophic falcine sinus, supplied by right posterior choroidal branches and small thalamoperforators (Figure 3A). The right transverse sinus is patent but drains anterograde to a venous plexus, while the left transverse sinus is atretic and only partially opacified from the left superior petrosal sinus. This differed from previous embolizations, where the patient demonstrated a dominant left transverse sinus which primarily drained the VOGM. The pathway for venous access to the malformation through the right transverse-sigmoid sinuses was small-caliber and tortuous. Considering the former dominance of the left sinus, recanalizing the atretic left side was considered as a more viable approach to obtain more direct venous access for TVE.

Figure 3.

(A) Subtracted AP angiogram of the left vertebral artery demonstrates the VOGM being supplied by the right posterior choroidal artery and thalamoperforating artery branches. The malformation drains into a hypertrophic falcine sinus. The left transverse sinus is atretic and not opacified. The right transverse sinus drains into the jugular vein and into a cavernous venous plexus. (B) Venous angiography after balloon angioplasty demonstrates the newly recanalized left transverse sinus with opacification and drainage to the left internal jugular vein. (C) Fluoroscopy demonstrates the placement of two stents in a telescoping fashion to maintain the integrity of the recanalized left transverse-sigmoid sinuses. (D) Venous angiography from the catheter placed in the straight sinus after stent placement demonstrates notably improved flow through the left transverse sinus. Venous outflow from the straight sinus no longer drains through the falcine sinus.

AP: angioplasty; VOGM: vein of Galen malformation.

After placing the 8Fr sheath in the left IJV, the triaxial system was used to traverse the occluded left transverse sigmoid sinus, and multiple angioplasties using a 5.5 mm × 2 cm balloon (Figure 3B) were performed. After sequential increases in diameter of the left transverse sinus, a 7Fr guiding catheter was navigated past the stenosed area to catheterize the straight sinus. TVE was performed by pressure cooker technique with complete obliteration of the malformation. To protect the recanalized left transverse sinus, two 8 × 36 mm Carotid Wallstents were deployed in a telescoping fashion across the left transverse-sigmoid sinus from the transverse sinus to the jugular foramen (Figure 3C). Multiple balloon angioplasties were performed in the jugular bulb to improve the wall apposition of the stents. Subsequent venograms demonstrated a redistribution of the posterior venous drainage from the falcine sinus to the bilateral transverse-sigmoid sinuses (Figure 3D).

The patient's postoperative course was complicated by a newly developed oculomotor nerve palsy considered secondary to inflammation from the embolic material and improving on dexamethasone. The patient was placed on aspirin 325 mg daily for his new stent and was safely discharged home. MRI at one-week follow-up demonstrated a patent stent without thrombosis or re-stenosis. Clinically, the patient noted improvement in his oculomotor symptoms.

Discussion

In these cases, we demonstrate the first successful placements of a venous sinus stent to normalize venous outflow after TVE of a VOGM, a high-flow cerebrovascular malformation, in three pediatric patients. Stents were placed to maintain the patency of stenotic dural venous sinuses and prevent a potentially disastrous re-stenosis or sinus thrombosis after curative TVE. These patients experienced no complications from placement of the stent, demonstrated excellent angiographic outcomes, and continued to have patent stents on clinical and radiographic follow-up. Angioplasty allowed for safe access by a transvenous approach even in patients who had a thrombosed or stenosed sinus. We were then able to stent the venous sinuses after the embolization of these patients to obliterate the malformation with restoration of normal arterial to venous blood flow. These initial results are encouraging, and further studies with larger sample sizes are warranted.

A major therapeutic goal of infantile VOGM embolization is relieving venous congestion.^1,4 The majority of the symptoms experienced by infants and children are secondary to hydrocephalus, rather than the combined neurological and cardiac presentation often seen in neonates. ¹⁵ Reducing venous hypertension by reducing the amount of shunting occurring through the malformation permits the reabsorption of cerebrospinal fluid, which is normally inhibited by the high venous pressure creating opposing force.^1,16 This in turn reduces the amount of hydrocephalus present in the infantile brain, decreasing compression and subsequent risk of cortical atrophy. If not managed appropriately, persistent venous congestion can lead to the development of collateral cortical drainage including the cavernous sinus and transosseous veins, which can clinically progress to developmental delays and failure to thrive in children.^17,18

In these three cases, concurrent stenosis of the transverse or sigmoid sinuses was present which further reduced venous outflow. Sinus stenosis is a known risk factor that complicates or entirely prevents transvenous access. Our group has previously described comorbid sinus stenosis as a notable feature of patients who present with VOGM: this may further exacerbate the symptomatic presentation of infants with VOGM. ¹¹ Venous sinus stenosis adds resistance to improve cardiac overload in neonatal VOGM, but drives further intracranial venous hypertension which worsens venous congestion. In Case 1, stenosis of the right sigmoid-jugular junction forced shunted blood to drain through the left transverse sinus and subsequently through cortical or subarachnoid pathways around the cerebellum. This pathologic drainage is a high-resistance vascular network which further exacerbated the degree of venous congestion experienced by the patient and would have made TVE riskier. The stenosis similarly complicated access, as all transarterial routes had been exhausted for safe embolization of the VOGM, and a typical guidewire and microcatheter assembly could not traverse the stenosis by a transvenous approach. After angioplasty and stent placement, angiography demonstrated that the majority of the blood was now preferentially draining through the stented right sigmoid sinus due to the now unfavorable resistance offered by the left dural sinuses.

Similar to typical indications for venous sinus stenting, venous angiography was the imaging method utilized to confirm stent placement as arteriograms provide an additional risk of generating distal emboli. Control angiographic runs were later performed to assess the overall post-embolization anatomy once patency of the stent and improvement of the vessel diameter and flow were demonstrated. Relief of stenosis for venous access was achieved by balloon angioplasty, so stent placement was not necessary while the VOGM was open and actively shunted blood. After normalization of cerebral blood flow by TVE, the stent was then placed for concern of exacerbated venous outflow restriction. Further studies are needed to assess the utility of stent placement while the VOGM is open and actively shunting, which may provide therapeutic benefits for patients with symptoms related to venous congestion.

The risk of worsening CHF after venous sinus stenting is a subject of ongoing concern. Venous sinus stenting decreases the outflow restriction in the posterior fossa dural sinuses leading to decreased intracranial venous hypertension, however, it also ultimately leads to increased cardiac overload.^2,11 In these cases, venous sinus stenting was performed in older children who are at decreased risk of CHF and therefore considered safer candidates for sinus stenting. Further studies directly assessing the risk of heart failure after venous sinus stenting are needed to better identify patients who are ideal candidates for this procedure.

Venous sinus stenting has been utilized in the pediatric cohort for relatively few indications. The main pediatric pathology that it has seen use in is as an alternative management option in refractory idiopathic intracranial hypertension (IIH) when it is associated with lateral sinus stenosis.^19,20 In these cases, venous manometry is performed during the endovascular procedure to ascertain that sinus pressures are elevated and that a trans-stenotic gradient of at least 4 mm Hg is present. ²¹ Recent meta-analyses demonstrate that VSS in adult IIH is safe and extremely effective, with a 94% rate of improvement in papilledema and a 90% rate of improvement in pulsatile tinnitus. ¹³ VSS has also seen use as a safe option for the management of isolated pulsatile tinnitus with associated lateral sinus stenosis. ¹⁴ Schwarz et al. ²² described a series of eight pediatric patients who received VSS for IIH intolerance to medication, did not respond to conservative or surgical management, or with fulminant disease. These patients were very symptomatic with noticeable effects on their quality of life; VSS resulted in symptomatic improvement without immediate complications, but had a re-stenting rate of 25% due to in-stent stenosis. However, the placement of a venous sinus stent does exhibit similar complications to TVE itself such as venous perforation, hemorrhage, and venous extravasation. ²³ The stent itself presents with its own related complications such as intraprocedural or delayed in-stent thrombosis and restenosis, exacerbated by the low-velocity flow conditions within the venous system. ²³ Stent placement also required initiation of antiplatelet therapy: in cardiac intervention for pediatric patients, single antiplatelet therapy with aspirin is considered sufficient to safely prevent thrombosis without increasing risk of postprocedural hemorrhagic complications. ²⁴ In our series, all patients received aspirin monotherapy for maintenance of their stent and demonstrated patency without complication on follow-up. Patient 1 received a second embolization after stent placement, which was successfully performed to obliterate the malformation without safety concerns or complications. Previous studies have shown that most vessel growth is completed within the first 4 years of life, so adult-sized venous sinus stents may be safely placed for pediatric IIH after 5 years of age. ²⁰ In our patients, we had no complications with placement of the stent and there was minimal concern for additional risk to the patient as we had already established transvenous access for the embolization. The patients continue to be monitored with serial imaging, but no long-term complication, need for stent resizing, or symptom recurrence has been identified to date.

In high-flow pathologies such as AVMs and AV fistulas, VSS has been utilized for the relief of high venous draining pressure with varied success previously. Tsumoto et al. ²⁵ described the placement of a sigmoid stent for clogged drainage of an AVM which initially had good outcomes, but subsequently restenosis within the stent that led to rupture of the AVM. Higgins and Kirkpatrick ²⁶ discussed palliative stenting of the straight sinus to relieve outflow congestion for an inoperable pontine AVM that led to noticeable symptomatic improvement. Hirata et al. ²⁷ described the placement of a VSS during TVE of a dural AV fistula for an acute intraprocedural venous sinus thrombosis that had a good clinical outcome for the patient. It is worth noting that in our placement of the stent, all patients had previously undergone staged TAE alongside the final TVE to reduce the degree of shunting through the VOGM as opposed to the placement of stents in patients receiving a first embolization as described by some cases in the literature. ²⁸ This normalized flow may have provided a relatively safe environment for the placement and long-term patency of the venous sinus stents.

Despite the excellent safety profile demonstrated for VSS in pathology in low or normal-flow conditions, there is limited prospective data to ascertain its safety in high-flow pathology. With our initial success in the long-term management of VOGM coupled with patent stents, further studies are warranted to appropriately assess the effectiveness of VSS as an adjunctive option in the management of high-flow pathologies. While successful, these three cases may not be representative of the larger population of patients with VOGM, and this may limit the generalizability of our findings. Future studies are also warranted to assess the utility of VSS as a therapeutic option for symptomatic relief in patients with venous congestion while the VOGM is actively being reduced.

Conclusion

We demonstrate long-term patency and management of potential post-TVE outflow restriction with the restoration of normal intracranial blood flow and excellent clinical outcomes by placement of a venous sinus stent after the TVE. In patients with VOGM and venous hypertension receiving TVE, venous sinus stenting may be a safe and effective option to reduce aberrant cortical venous drainage and improve normal outflow. TVE should still be considered as a treatment option even in pediatric patients with comorbid occluded venous sinuses. Further studies with larger sample sizes are necessary to further elucidate the safety and efficacy of this adjunctive option.