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J Neurosurg Case Lessons
J Neurosurg Case Lessons
J Neurosurg Case Lessons
Journal of Neurosurgery: Case Lessons
2694-1902
American Association of Neurological Surgeons

39186822
10.3171/CASE24182
CASE24182
Endovascular-NeurosurgeryEndovascular NeurosurgeryPediatricPediatricVascular-DisordersVascular DisordersCase Lesson
Endovascular management of pediatric pial arteriovenous fistulas with hereditary GDF2 mutation: illustrative case
Hu Hui MD 1
Chen Hao MD 1
Li Lusheng MD, PhD 123
Zhai Xuan MD, PhD 123
Liang Ping MD 123
Tang Jun MD, PhD 123
1 Department of Neurosurgery, Children’s Hospital of Chongqing Medical University, Chongqing, China
2 National Research Center for Child Health and Disorders, Chongqing, China
3 Chongqing Key Laboratory of Translational Medical Research in Cognitive Development, Learning, and Memory Disorders, Chongqing, China
Correspondence Jun Tang: Children’s Hospital of Chongqing Medical University, Yu Bei District, Chongqing, The People’s Republic of China. tangjun@hospital.cqmu.edu.cn.
INCLUDE WHEN CITING Published August 26, 2024; DOI: 10.3171/CASE24182.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

26 8 2024
26 8 2024
8 9 CASE2418215 3 2024
11 6 2024
© 2024 the authors
2024
the authors
https://creativecommons.org/licenses/by-nc-nd/4.0/ CC BY-NC-ND 4.0 (http://creativecommons.org/licenses/by-nc-nd/4.0/)

BACKGROUND

Intracranial pial arteriovenous fistulas (PAVFs) are uncommon neurovascular anomalies that primarily affect the pediatric population. PAVFs are often linked to hereditary hemorrhagic telangiectasia, yet the specific genetic mutations remain unidentified. While endovascular embolization is the preferred treatment for PAVFs, complications like hydrocephalus and sinus thrombosis pose challenges in management.

OBSERVATIONS

The authors present a rare case of PAVF in a 6-month-old male neonate with a hereditary GDF2 mutation, where the fistula was supplied by the posterior inferior cerebellar artery and drained directly into the sigmoid sinus. The PAVF was effectively treated with endovascular embolization using coils and Onyx. Furthermore, the authors describe the successful use of rivaroxaban in managing subsequent sinus thrombosis after the embolization of PAVFs. Additionally, the authors review treatment strategies and complications following fistula disconnection.

LESSONS

Endovascular embolization is the primary treatment choice for the majority of pediatric PAVFs, while a hereditary GDF2 mutation is considered a potential contributing factor to the formation of these malformations in children. Rivaroxaban has shown promise as an effective therapeutic option for pediatric sinus thrombosis, supported by its established safety profile.

https://thejns.org/doi/10.3171/CASE24182

pediatric
PAVF
GDF2 mutation
sinus thrombosis
rivaroxaban
ABBREVIATIONS

AVM = arteriovenous malformation
BOT = balloon occlusion test
CNV = copy number variation
CSF = cerebrospinal fluid
CT = computed tomography
CTA = CT angiography
CVT = cerebral venous thrombosis
DSA = digital subtraction angiography
HHT = hereditary hemorrhagic telangiectasia
MRI = magnetic resonance imaging
NBCA = N-butyl-cyanoacrylate
PAVF = pial arteriovenous fistula
PICA = posterior inferior cerebellar artery
TAE = transarterial embolization
VGAM = vein of Galen malformation
WES = whole-exome sequencing.
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pmcIntracranial pial arteriovenous fistulas (PAVFs) are rare neurovascular lesions characterized by a direct shunt between the pial feeding arteries and the draining vein without a true nidus. It has been reported that PAVFs occur in 7.3% of all cerebral arteriovenous malformations (AVMs) in the pediatric population and in 1.6% in the general population.1 Congenital PAVFs are frequently associated with congenital diseases in childhood and present complications, including mass effect, cognitive cardiac failure, hemorrhage, venous hypertension, hydrocephalus, and focal neurological deficits.2, 3 Pediatric PAVFs have a strong association with hereditary hemorrhagic telangiectasia (HHT), but the genetic mutations involved are not fully understood.4, 5 The natural history of PAVFs is not well known, and only 1 case of spontaneous thrombosis has made the pediatric fistula indiscernible. Endovascular therapy via transarterial embolization (TAE) is considered the first-line therapy for PAVFs in contemporary practice, but treatment strategies for complications such as hydrocephalus and venous hypertension remain controversial.6 Researchers have reported poor outcomes, with a reported mortality rate of 63% in patients with untreated PAVFs.7

Here, we report the rare case of a PAVF supplied by the posterior inferior cerebellar artery (PICA) and draining directly into the sigmoid sinus in a 6-month-old male infant with a hereditary GDF2 mutation. Furthermore, we present the first documented case demonstrating the efficacy of rivaroxaban in managing consequential sinus thrombosis following the successful embolization of PAVFs.

Illustrative Case

A 6-month-old boy was referred to our hospital because of paroxysmal seizures lasting a few seconds. Two weeks before the first seizure attack, the child experienced no significant disturbances. A computed tomography (CT) scan revealed encephalatrophy and broadening of the subarachnoid space (Fig. 1A). To better visualize the cerebral artery, CT angiography (CTA) scans were obtained, which revealed significant bilateral transverse sinus dilation, cortical venous enlargement, and an uncertain snakelike aneurysm in the posterior fossa (Fig. 1B and C). Cardiac ultrasound revealed no significant heart failure. After a routine examination, the infant underwent digital subtraction angiography (DSA), which revealed no sinus congestion or cortical venous congestion when the catheter was in the right internal carotid artery (Fig. 1D). Angiography of both vertebral arteries confirmed that a PAVF was supplied by an aneurysmal single branch of the left vertebral artery and drained into the dilated sigmoid sinus with retrograde reflux to the contralateral transverse sinus, sagittal sinus, and cortical veins. Moreover, there were stenoses in both sigmoid sinuses, especially in the left sigmoid sinus (Fig. 1E–G). FIG. 1. Preoperative brain CTA and first DSA images. Axial CT scan (A). Axial (B) and sagittal (C) CTA images revealed a dilated transverse sinus. Venous phase DSA of the right internal carotid artery (D). Arterial phase DSA of the right and left cerebellar arteries (E and F). Axial view of a double image of the posterior circulation (G).

Because we could not confirm that the feeding artery was the left PICA, we performed a balloon occlusion test (BOT) with a balloon (Hyperform, Medtronic) through the left vertebral artery and captured the entire visible basilar artery and all branches on angiography of the right vertebral artery (Fig. 2A and B). Following confirmation of a single-hole PAVF supplied by the aneurysmal PICA, the PICA aneurysm and fistula were excluded from the cerebral circulation by TAE using coils and Onyx (ev3 Neurovascular; Fig. 2C and D). Immediate angiography revealed no signs of the PICA aneurysm or PAVF, with proximal PICA protection and visible basilar artery (Fig. 2E). Most importantly, we detected the anterograde reflux of blood in the venous system, even though the sinus stenoses still existed and did not expand with the balloon (Fig. 2F). FIG. 2. DSA images obtained during endovascular embolization. A: Balloon catheter in the left PICA position. B: Angiography through the right cerebellar artery after ballooning (black arrow). C: The aneurysmal sac and fistula were coiled. D: Glue was injected after coiling. E: Immediate angiography after embolization. Black arrowhead indicates the occlusive site. F: Venous phase angiography immediately after embolization. The red arrows indicate stenosis of the left sigmoid sinus and free drainage of the right sigmoid sinus.

The infant recovered well from the anesthesia, and no seizures occurred following embolization. Three days after surgery, the child presented with remarkable psychomotor retardation and decreased appetite. CT and magnetic resonance imaging (MRI) revealed a dilated ventricle (Fig. 3A–C) and venous thrombosis (Fig. 3E) located in the bilateral transverse sinus. A two-step strategy was adopted. The child underwent Ommaya device implantation first for temporary drainage of cerebrospinal fluid (CSF), followed by anticoagulation with 5 mg of rivaroxaban orally for 3 months. The child was discharged on the 10th day following temporary drainage without any complications. At the 6-month follow-up, MRI revealed normal ventricles and no sinus thrombosis (Fig. 3D, F, and G). During rivaroxaban treatment, blood tests revealed no abnormalities, and no bleeding complications occurred. FIG. 3. CT and MRI 3 days (3d) after embolization (emb.) and at the 6-month (6mo.) follow-up. A–C: Axial and sagittal CT and MR image showing a significantly dilated ventricle. E: Axial T1-weighted MRI showing thrombosis in the transverse sinus 3 days after embolization. D andF: Axial T1- and T2-weighted MRI at 6 months of follow-up, revealing induced hydrocephalus and sinus thrombosis vanishing. G: Magnetic resonance venography showing free drainage of the right sigmoid sinus and stenosis in the left sigmoid sinus.

To understand the etiology of this rare PAVF, we collected peripheral blood from the child and his parents for whole-exome sequencing (WES) and whole-genome copy number variation (CNV) analysis. Bioinformatic analysis revealed a missense mutation containing a 37-bp region located on chromosome 10 (10q11.22q11.23), including the GDF2 variant chr10:48414516 (OMIM:615506). Integrative Genomics Viewer analysis confirmed that the missense mutation of the GDF2 variant was inherited from his mother (Fig. 4). FIG. 4. WES and whole-genome CNV analysis. A: GDF2 variant of the family according to WES analysis. B: Family tree for the GDF2 mutation.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

PAVFs are rare and consist of abnormal direct arterial-to-venous shunts without an intervening nidus. PAVFs develop in the subpial meningeal space and are classified as single holes or multiple holes according to the number of feeding arteries involved.3 Distinct from vein of Galen malformations (VGAMs), nongalenic PAVFs are characterized by the absence of involvement of the embryonic median prosencephalic vein of Markowski.8 The rate of PAVFs is low, at 1.6%–4.7%, and their natural history is poorly understood due to the limited number of cases.9 PAVFs are frequently associated with HHT, but the genetic mutations involved are unclear. Endovascular embolization has been proven to be the preferred choice for managing PAVFs, but complications such as hydrocephalus and sinus thrombosis are difficult to manage.

Pediatric PAVFs and HHT

HHT is known as an inherited blood vessel disease associated with genetic deficits in the transforming growth factor-β (TGF-β) gene. Generally, mutations in SMAD4 (MIM600993), ALK (MIM601284), and endoglin (MIM 131195) are responsible for HHT1, HHT2, and juvenile polyposis HHT, respectively.9 Studies have suggested that there are still undiscovered genetic mutations associated with HHT, as approximately 15% of patients with HHT currently have no known genetic mutations. Because of its rare morbidity, the etiology of PAVF remains unknown. Recent case series reported that nongalenic PAVFs account for 7.3%–8.4% of AVMs in the pediatric brain and that HHT is observed in 8%–16% of AVMs.9, 10 Here, we present the rare case of a PAVF fed by the PICA in a 6-month-old male infant with a hereditary GDF2 mutation. His mother had 2 marriages, and her first child with an ex-husband died of unknown reasons. No physical dysfunctions were detected in the mother, and she refused to undergo imaging examinations of the brain and vascular system. Using Integrative Genomics Viewer analysis, we confirmed that the child and his mother had the same missense mutation of the GDF2 variant. To our knowledge, this is the first report showing that a confirmed hereditary missense mutation in a GDF2 variant is correlated with PAVF in the pediatric brain. GDF2, responsible for encoding bone morphogenetic protein-9, is also associated with an HHT-like phenotype. Recent findings have linked pulmonary arterial hypertension and pulmonary AVMs to GDF2-related HHT. In a study by Ma et al., a complete fetal posterior cerebral artery was observed in an adult patient with a missense mutation of the GDF2 variant.11 Overall, the hereditary GDF2 mutation is likely a pathogenic factor for this pediatric PAVF, which should be considered when the parents decide to have another baby.

Pediatric PAVF Treatment in the Literature

The aim of PAVF treatment in children is to improve clinical symptoms, preserve normal neurocognitive maturation, and protect against progressive neurological deficits and hemorrhage. Comprehensive angioarchitectural analysis of PAVFs is crucial for decision-making regarding treatment strategies. Both surgical and endovascular embolization are effective at controlling arteriovenous shunts.12 Recent reports indicate that conservative therapy results in high mortality and hemorrhage.7 Due to technological improvements and the growing experience of neurosurgeons and neuroradiologists, endovascular embolization has become the first-line treatment for most PAVFs, especially in children and neonates, because of its low invasive potential.13 A transarterial approach is preferred in children, although transvenous embolization for VGAMs and dural AVFs is possible. The transvenous approach carries a greater risk of complications with immediate or delayed hemorrhage because of high intravenous pressure. Surgical indications for PAVF are limited in pediatric patients because of increased compensatory brain damage and decreased blood volume. Surgery should be considered if endovascular embolization fails or if the patient could not survive with a “wait-and-see” strategy.13 In the present case, we embolized the single hole via a transarterial approach with bilateral femoral artery puncture because the BOT technique was used to ensure the integrity of the posterior circulation after fistula occlusion and the small cerebral artery could not bear a 6-Fr or larger microcatheter. In addition, a transvenous approach was applied if we expanded the stenosis of the sigmoid sinus with a balloon, and we abandoned this strategy because of unexpected risks. Several materials, such as N-butyl-cyanoacrylate (NBCA), coils, and Onyx, have been reported to be effective at embolizing fistulas and aneurysmal arteries.1 NBCA is generally used for high-flow fistulas and multiple holes because the adhesive agent can prevent the migration of the mixture into the lung. Coils are often used to embolize aneurysmal arteries and, together with embolic agents, to solidify the embolization and prevent extra migration. Onyx, a nonadhesive liquid embolic agent, is generally used for single-hole fistulas and is combined with coils. Here, we used coils to embolize the aneurysmal PICA but not the distal fistula to avoid hemorrhagic risk during the procedure when the fistula was occluded. Onyx was used to completely block the flow, and extra backflow was avoided to protect the proximal perforator vessels of the PICA. No standard treatment strategies for PAVF exist because of the variety of relevant feeding arteries and drainage veins; thus, a case-by-case evaluation should be adopted.

Venous Thrombosis Following Fistula Disconnection

Complications associated with PAVF have been well discussed,1 but few studies have reported complications following fistula disconnection (Table 1), especially venous thrombosis, and treatment strategies in pediatric patients. Regardless of the surgical or interventional approach, fistula disconnection of the PAVF can result in progressive thrombosis of the drainage veins, leading to brain edema, hydrocephalus, and even cerebral hematoma.14–16 Lv et al. reported that 20% (3/16) of hydrocephalus cases were caused by venous thrombosis after fistula occlusion.17 We speculate that 2 possible mechanisms for postoperative thrombosis and hydrocephalus may be as follows: 1) the sudden occlusion of a high-flow PAVF can reduce blood flow in the dilated sinus, followed by sinus thrombosis. 2) Thrombosis can increase sinus pressure, leading to the blockage of CSF reabsorption, which can result in detrimental venous infarction or hemorrhage. Yang et al. encountered symptomatic venous infarction in a 13-year-old child 3 days after surgical ligation of a left temporal PAVF.18 Lv et al. reported 3 of 16 patients with venous infarction or hemorrhage after complete embolization of the PAVF, and all 3 patients received no heparin treatment.17 These authors recommended that heparin be given routinely after endovascular embolization.19 Achieving an activated clotting time of twice the normal level during the first 24 hours after embolization was the goal in patients with headaches, and then they received low-molecular-weight heparin for 15 days. However, Ye and Zhang administered low-molecular-weight heparin only to patients diagnosed with symptomatic venous thrombosis, and the CT scan did not show intracranial hemorrhage.20 Most of the reports have proven the effectiveness of heparin in improving venous thrombosis postoperatively, but few have investigated its safety and effectiveness in pediatric patients. A recent randomized trial (NCT02234843, ClinicalTrials.gov) revealed that rivaroxaban or a standard anticoagulant (heparin) had a low risk of recurrent and clinically relevant bleeding in children with cerebral venous thrombosis (CVT).21 The authors found that rivaroxaban administration resulted in 25% complete or 53% partial sinus recanalizations of CVT, while the rates in standard anticoagulant recipients were 15% and 59%, respectively. Here, we encountered serious sinus thrombosis and hydrocephalus in a 6-month-old boy after complete embolization of the PAVF. The child underwent Ommaya device implantation first for temporary drainage of CSF, followed by anticoagulation with 5 mg of rivaroxaban orally for 3 months. The complete recovery and the disappearance of sinus thrombosis on MRI during follow-up provide a new strategy and effective medication for pediatric CVT following PAVF disconnection. TABLE 1. Reported cases with postoperative anticoagulation of PAVF

Authors & Year	Sex/Age (yrs)	Symptoms	Fistula	Feeding Artery	Treatment	Mos of Follow-up	Postop Complications	Antithrombosis	Outcome
	
Coubes et al., 199614	F/13	Subacute posterior neck pain & ataxia	Single hole	Rt vertebral artery	Embolization w/ NBCA	12	Venous thrombosis	Postop w/ heparin (100 mg/day) for 5 days	Free of symptoms & complete occlusion of fistula	
Yang et al., 201318	–/13	Generalized tonic seizure	Dual hole	Lt MCA & lt PCA	Ligated w/ aneurysm clip	6	Cerebral edema	Postop day 3 w/ anticoagulation & antiplatelet	Near disappearance of cerebral edema & complete occlusion of fistula	
Ji et al., 201615	M/37	Seizures for 4 mos	—	Lt MCA & rt PCA	Endovascular coil embolization	5	Rapid progressive venous thrombosis & ICH	Intraop & postop w/ heparin for 2 days	No evidence of intracranial hemorrhage, DSA showed complete occlusion of 2 PAVFs	
Lv et al., 201017	7 F, 9 M/mean 18 (range 2–44)	6 ICH, 6 headaches, 2 seizure, 1 neurological deficit, 1 transient ischemic attack	—	6 MCA, 4 ACA, 3 PCA, 2 BA, 1 PICA	1 Onyx-34, 10 detachable coils, 2 detachable coils & Onyx-34, 1 detachable coil & 34% NBCA, 1 free coil & 20% NBCA, 1 fiber coil	Mean 7.4 (range 3–12)	Venous thrombosis	Intraop w/ heparin	GOS score: 15 w/ score V, 1 w/ score IV	
Gonzalez et al., 201316	M/15	—	Single hole	ICA	Surgical clip	—	Straight sinus thrombosis	Intraop intravenous injection of heparin, postop infusion of tPA when venous thrombosis	Brain death 72 hrs after initial procedure	
Ye et al., 201820	2 F, 6 M/mean 19.4 (range 1–48)	4 seizure, 3 headache, 1 subarachnoid hemorrhage	Single hole	2 A2, 1 M1, 2 M2, 1 M3, 1 P1, 1 PICA	Transarterial balloon-assisted glue embolization	Mean 12.1 (range 6–32)	2 cases of venous thrombosis, drainage vein & sinus	Intraop IV heparin w/ bolus dose of 0.5 mg/kg	Good (mRS score 0)	
Lv et al., 200919	2 F, 7 M/mean 17.8 (range 2–40)	4 ICH, 2 headaches, 1 seizure, 2 no symptoms	—	4 ACA, 1 MCA, 2 PCA, 1 BA	7 detachable coils, 1 Onyx-34, 1 combination of coils & NBCA	Mean 5.7 (range 3–12)	3 cases of spontaneous thrombosis	Intraop & postop w/ heparin for 2–15 days until headaches alleviated	Good (mRS score 0)	
Present case	M/0.5	Seizure	Single hole	PICA	Embolization w/coils & Onyx	6	Transverse sinus thrombosis/hydrocephalus	Postop 5 mg rivaroxaban orally for 3 mos	Good (mRS score 0), disappearance of thrombosis & normal ventricle	
ACA = anterior cerebral artery; BA = basilar artery; GOS = Glasgow outcome score; ICA = internal carotid artery; ICH = intracranial hemorrhage; IV = intravenous; mRS = modified Rankin scale; MCA = middle cerebral artery; PCA = posterior cerebral artery; tPA = tissue plasminogen activator.

Limitations

It is important to acknowledge the lack of long-term follow-up data, potential challenges in generalizing specific management decisions to all patients with similar conditions, and the inherent risks of anticoagulation therapy, particularly in pediatric patients. Additionally, the interpretation of the GDF2 mutation’'s pathogenicity and its direct relevance to the patient’s condition may be limited without additional functional studies or genetic counseling. These limitations underscore the need for further research and careful consideration of individual patient factors in treatment planning.

Lessons

Endovascular embolization with coils, glue, balloon catheters, or other agents has been proven to be the first-level treatment strategy for pediatric PAVFs. Here, we report a patient with a surgically embolized PICA–sigmoid sinus fistula with a hereditary GDF2 mutation. In addition, we present the first case of successfully managed sinus thrombosis following occlusion of a pediatric PAVF with rivaroxaban administration. More studies on the safety and effectiveness of rivaroxaban for treating venous thrombosis following fistula disconnection are needed.

Acknowledgments

This work was funded as a general project of the Natural Science Foundation Chongqing (cstc2021jcyj-msxmX0606, J.T.) and the China Postdoctoral Science Foundation (2020M683757, J.T.).

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Tang, Zhai, Liang. Acquisition of data: Tang, Hu, Li, Zhai. Analysis and interpretation of data: Hu, Chen, Li, Liang. Drafting the article: Tang, Hu, Chen, Li. Critically revising the article: Tang, Li, Zhai. Reviewed submitted version of manuscript: Tang, Hu, Chen, Zhai, Liang. Approved the final version of the manuscript on behalf of all authors: Tang. Statistical analysis: Chen. Administrative/technical/material support: Zhai. Study supervision: Tang, Liang.

Correspondence

Jun Tang: Children’s Hospital of Chongqing Medical University, Yu Bei District, Chongqing, The People’s Republic of China. tangjun@hospital.cqmu.edu.cn.
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