Vein of Galen Aneurysmal Malformation: Advances in Management and Endovascular treatment

Vein of Galen Aneurysmal Malformation: Advances in Management and Endovascular treatment Abstract BACKGROUND Vein of Galen aneurysmal malformation (VGAM) is a rare congenital vascular malformation representing <1% of all arteriovenous malformations. The knowledge and strategies in the management are constantly evolving. OBJECTIVE To review our series of postneonatal VGAM patients treated over 11-yr period. METHODS Retrospective analysis of 113 VGAM treated between January 2004 and April 2015. After exclusions, 45 patients were included: 33 choroidal and 12 mural types. RESULTS Presenting symptom in the order of frequency: enlarged head circumference, antenatal diagnosis, mild CHF, and PHT at birth. Older patients were diagnosed following trauma, headache, cognitive decline, and incidentally during workup for other diseases. Hydrocephalus due to hydrodynamic disorder was present in 70% of choroidal and 58% of mural types. Only a quarter needed cerebrospinal fluid diversion procedure. Radiological cure was achieved in 82%; the outcome graded on a 5-point scale: 0 (death) to 4 (normal). A total of 66.6% are neurologically and developmentally intact with outcome score 4, 20% had outcome score of 3, and 8.9% had outcome score of 2. There was 4.4% mortality. Dural feeders to VGAM were found either in the initial or during the treatment in 22.2% in the current series. Angiogenesis from pial vessels developed after partial embolization in 17.7% that resolved completely following complete obliteration of VGAM. CONCLUSION Technical and technological advancements in endovascular embolization along with better understanding of clinical, anatomic, and pathophysiological aspects have resulted in significantly improved outcome and prognosis in VGAM. Most patients with proper treatment can now survive and most develop normally following appropriately timed treatment. Vein of Galen, AV Malformation, AV fistula, Endovascular embolization ABBREVIATIONS ABBREVIATIONS AVM arteriovenous malformation CHF congestive heart failure CM capillary malformation CSF cerebrospinal fluid DSA digital subtraction angiography ICA internal carotid artery MRA magnetic resonance angiography MRI magnetic resonance imaging n-BCA N-butyl-cyanoacrylate NCCT noncontrast computed tomography PHT pulmonary hypertension USG ultrasonogram VGAD vein of Galen aneurysmal dilatation VGAM vein of Galen aneurysmal malformation Vein of Galen aneurysmal malformation (VGAM) is a rare congenital vascular disorder representing less than 1% of all arteriovenous malformations (AVMs) in the cooperative study of subarachnoid hemorrhage.1-3 The exact incidence is difficult to determine, as there is significant diagnostic confusion among various malformations that cause dilatation of the vein of Galen or its embryonic precursor. VGAM is located in the subarachnoid space in the choroid fissure and embryologically related to the development of the choroid plexus as demonstrated by Raybaund et al in 1989.4 The concept of this disease was further elucidated by Berenstein et al5 and Garcia-Monaco et al,6 who defined VGAM as arteriovenous fistulas draining to the embryonic precursor of the vein of Galen called median vein of prosencephalon. These studies subclassified VGAM further into choroidal and the mural types. Other vascular lesions including pial or dural arteriovenous malformation that cause dilatation of the “true” (embryologically matured) vein of Galen were designated as vein of Galen aneurysmal dilatation (VGAD). Vein of Galen varix is a dilated vein of Galen without arteriovenous shunts.5 The knowledge and strategies in the management of VGAM are constantly evolving. We reviewed our series of postneonatal VGAM patients treated over an 11-yr period and have discussed the presentation, management strategies, results, and clinical outcome. METHODS We retrospectively reviewed the patients with dilated vein of Galen treated at our center between January 2004 and April 2015. Appropriate institutional review board approval was obtained for retrospective review of the nonidentifiable patient information and appropriate patient consent obtained. We categorized them as VGAM of either choroidal or mural types and VGAD. We also categorized them based on the timing of treatment as neonatal and older. For the study purpose we excluded, VGAM treated partly before 2004, VGAM treated at outside institution before we took over the care, VGAD, and VGAM treated in the neonatal period were excluded, as we have reported them previously.7 We gathered clinical information and procedure details from the patient chart, reviewed the images for categorization and analysis of outcome. The referring physician and/or the patient family was called to find the current functional activity using a standardized age appropriate questionnaire. They were then graded on a 5-point scale suggested by Jones et al,8 ranging from 0 (death) to 4 (normal). Children having severe neurological impairment, requiring intensive supportive care and medical management were given a score of 1. Presence of moderate neurological impairment affecting activities of daily living and requiring significant support in educational and social interactions but a lesser degree of daily medical management were given a score of 2. Children who had milder degree of impairment, resulting in some need for social and educational support, with medical management only on occasion were a given score of 3.8 RESULTS In total, we reviewed 113 patients with enlarged vein of Galen treated at our center between January 2004 and April 2015. We excluded 23 patients with treatment initiated before 2004 as we did not have the complete set of images for review. We excluded 14 patients initially treated at outside institution as the initial management strategy was different from ours and most of them were referred following a clinical complication. We excluded the VGAM treated in the neonatal period (21 patients) as we have published a series previously.7 We also excluded 10 patients with VGAD that will be reported separately. After exclusion, we had a subset of 45 patients of VGAM that presented to and treated by our team from the beginning (Table 1). TABLE 1. Overview of Our Series of Cases Treated Between January 2004 and April 2015 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 View Large TABLE 1. Overview of Our Series of Cases Treated Between January 2004 and April 2015 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 View Large Of the 45 patients selected for the analysis, 33 were choroidal and 12 were mural type. Among 33 choroidal VGAM, M:F ratio was 17:16, and among the 12 mural VGAM, M:F ratio was 7:5. The most common presenting symptom was progressive increased head circumference and antenatal diagnosis with scans followed by mild congestive heart failure and pulmonary hypertension at birth that was managed medically. Other patients were diagnosed following scans done for trauma to head, and others presented with headache, cognitive decline, and incidentally during workup for other diseases (Table 2). TABLE 2. Clinical Presentation of Each of Our Cases Along With Segregation Into the Choroidal and Mural types of VGAM S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 View Large TABLE 2. Clinical Presentation of Each of Our Cases Along With Segregation Into the Choroidal and Mural types of VGAM S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 View Large Analyzing the timing of diagnosis, a significant number of patients were diagnosed antenatally with USG followed by fetal magnetic resonance imaging (MRI), but majority of patients in the study group were diagnosed in neonatal, infancy, and early childhood (Table 3). In our series, all mural and most choroidal VGAM were diagnosed before 12 mo of age. All the patients selected for the analysis here were either stable or managed medically in the neonatal period. Based on our protocol, the VGAM known since birth were periodically followed both clinically and radiologically till 6 mo of age when definitive treatment was initiated. Most of our patients were treated during infancy as planned (Table 3). However, in the subgroup analysis among the 6 patients presenting with CHF and PHT in the neonatal period that were managed medically, 5 developed hydrovenous dysfunction before 6 mo of age and were treated by endovascular embolization, while among the 12 patients diagnosed antenatally and were born without CHF, only 3 patients needed endovascular embolization earlier than 6 mo. TABLE 3. The Data Depicts the Time of Clinical Presentation and the Timing of Treatment in Choroidal and Mural-Type VGAM Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 View Large TABLE 3. The Data Depicts the Time of Clinical Presentation and the Timing of Treatment in Choroidal and Mural-Type VGAM Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 View Large Hydrocephalus due to hydrodynamic disorder manifested as ventricular and cerebrospinal fluid (CSF) space enlargement associated with VGAM is common. In the current series, 23 out of 33 patients with choroidal type (70%) had hydrodynamic hydrocephalus. Only 6 of them underwent venriculoperitoneal shunt placement and 2 had endoscopic third ventriculostomy. Seven of 12 patients with mural type of VGAM had hydrocephalus (58%). None of these patients were treated by CSF diversion procedure. Overall, two-thirds (66.6%) of the patients presented with hydrocephalus and among them only one-fourth of them (26.6%) needed special procedure for CSF diversion, rest of the patients were managed by reducing the hydrovenous pressure by embolization. Among the 45 patients, in 37 (82%) we achieved radiological cure of the malformation and 6 patients (13.3%) are still under treatment (Table 4). To achieve this cure, choroidal VGAM (Figures 1 and 2) had between 2 and 11 procedures per patient with an average of 4.3 procedures, while mural VGAM (Figure 3) had between 1 and 8 procedures per patient with an average of 2.9 procedures per patient. FIGURE 1. View largeDownload slide Child born of a full-term normal delivery presented with prominent facial veins along with macrocephaly and developmental regression. A-D, At 10 mo of age he was diagnosed with VGAM. Brain CT and MRI show the enlarged vein of Galen (A and B) and its enlarged choroidal feeding vessels (C and D). E and F, Digital subtraction angiography (DSA) of left vertebral artery reveals enlarged bilateral posterolateral choroidal arteries feeding the VGAM. G and H, DSA of left internal carotid artery (ICA) reveals an enlarged anterior choroidal artery supplying the VGAM, and the venous phase shows narrowing of the falcine sinus and nonmaturation of jugular bulb on either side. I and J, DSA of the right ICA reveals additional supply through enlarged anterior cerebral artery into the enlarged remnant of median vein of procencephalon constituting the malformation. K and L, Superselective microcatheter angiogram through the left anterior choroidal artery reveals the enlarged feeder, large fistula opening into the malformation. FIGURE 1. View largeDownload slide Child born of a full-term normal delivery presented with prominent facial veins along with macrocephaly and developmental regression. A-D, At 10 mo of age he was diagnosed with VGAM. Brain CT and MRI show the enlarged vein of Galen (A and B) and its enlarged choroidal feeding vessels (C and D). E and F, Digital subtraction angiography (DSA) of left vertebral artery reveals enlarged bilateral posterolateral choroidal arteries feeding the VGAM. G and H, DSA of left internal carotid artery (ICA) reveals an enlarged anterior choroidal artery supplying the VGAM, and the venous phase shows narrowing of the falcine sinus and nonmaturation of jugular bulb on either side. I and J, DSA of the right ICA reveals additional supply through enlarged anterior cerebral artery into the enlarged remnant of median vein of procencephalon constituting the malformation. K and L, Superselective microcatheter angiogram through the left anterior choroidal artery reveals the enlarged feeder, large fistula opening into the malformation. FIGURE 2. View largeDownload slide View largeDownload slide (Continuation of the images from Figure 1). A and B, Superselective microcatheter angiogram through the anterior cerebral artery reveals another large feeder draining into the malformation. C, Glue cast at the end of first embolization session. D, The residual shunt is shown with right ICA angiogram at the end of first embolization session. E and F, Six months later second procedure was performed, the residual shunt is seen. Further embolization of few pedicles from right and left posterolateral choroidal arteries was performed. G and H, At the end of second embolization procedure, the flow to the malformation was significantly reduced with good blood flow to the brain tissue. I-N, Six-month follow-up angiograms of the right ICA, left ICA, and left vertebral artery reveal complete obliteration of the VGAM. O and P, MRI brain reveals complete obliteration, and normal development of the brain and MRA show the normal vasculature. FIGURE 2. View largeDownload slide View largeDownload slide (Continuation of the images from Figure 1). A and B, Superselective microcatheter angiogram through the anterior cerebral artery reveals another large feeder draining into the malformation. C, Glue cast at the end of first embolization session. D, The residual shunt is shown with right ICA angiogram at the end of first embolization session. E and F, Six months later second procedure was performed, the residual shunt is seen. Further embolization of few pedicles from right and left posterolateral choroidal arteries was performed. G and H, At the end of second embolization procedure, the flow to the malformation was significantly reduced with good blood flow to the brain tissue. I-N, Six-month follow-up angiograms of the right ICA, left ICA, and left vertebral artery reveal complete obliteration of the VGAM. O and P, MRI brain reveals complete obliteration, and normal development of the brain and MRA show the normal vasculature. FIGURE 3. View largeDownload slide View largeDownload slide Child born of a full-term normal delivery developed increased head circumference and prominent facial and scalp veins at 7 mo of age. Evaluation with CT scan brain (A) and MRI brain (B) reveals VGAM with significantly enlarged ventricular system. C, Prominent facial and scalp veins. DSA examination of left vertebral artery (D) and (E), right ICA (F–H), and left ICA (I) and (J) reveals a mural type of VGAM. The images also reveal that the vein of Galen sac is significantly enlarged with narrowing of falcine sinus and enlargement of superior sagittal sinus. There is also dysmaturation of the jugular bulb resulting in collateral venous drainage along scalp and facial veins. H, Collateral venous drainage following right ICA angiogram. K and L, Microcatheterization and superselective angiogram reveal a single-hole high-flow fistula. M and N, Glue case for glue injection under systemic hypotension. O and P, Immediate postembolization angiogram reveals complete obliteration of the malformation. The child head circumference stabilized and the enlarged facial and scalp veins became less prominent over time and the child achieved normal developmental milestones. Q-T, Six-month follow-up angiogram reveals persistent complete obliteration of the malformation. U, Follow-up CT brain reveals normal development of the brain with stable ventricular size. FIGURE 3. View largeDownload slide View largeDownload slide Child born of a full-term normal delivery developed increased head circumference and prominent facial and scalp veins at 7 mo of age. Evaluation with CT scan brain (A) and MRI brain (B) reveals VGAM with significantly enlarged ventricular system. C, Prominent facial and scalp veins. DSA examination of left vertebral artery (D) and (E), right ICA (F–H), and left ICA (I) and (J) reveals a mural type of VGAM. The images also reveal that the vein of Galen sac is significantly enlarged with narrowing of falcine sinus and enlargement of superior sagittal sinus. There is also dysmaturation of the jugular bulb resulting in collateral venous drainage along scalp and facial veins. H, Collateral venous drainage following right ICA angiogram. K and L, Microcatheterization and superselective angiogram reveal a single-hole high-flow fistula. M and N, Glue case for glue injection under systemic hypotension. O and P, Immediate postembolization angiogram reveals complete obliteration of the malformation. The child head circumference stabilized and the enlarged facial and scalp veins became less prominent over time and the child achieved normal developmental milestones. Q-T, Six-month follow-up angiogram reveals persistent complete obliteration of the malformation. U, Follow-up CT brain reveals normal development of the brain with stable ventricular size. TABLE 4. The Overall Outcome of Treatment in Choroidal and Mural Types are Represented. The Cure Mentioned Here Means the Angiographic Cure Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 View Large TABLE 4. The Overall Outcome of Treatment in Choroidal and Mural Types are Represented. The Cure Mentioned Here Means the Angiographic Cure Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 View Large In the 45 patients with VGAM, there were 2 deaths (4.4% mortality). Among the rest that include radiologically cured and patients still undergoing treatment in stages, 30 patients (66.6%) were neurologically and developmentally intact with an outcome score of 4. Nine patients (20%) had outcome score of 3 with mild impairment, and 4 patients (8.9%) had outcome score of 2 with moderate impairment of function. Dural feeders to the VGAM were found either initially or during the course of treatment in 22.2% of patients in the current series. Angiogenesis from pial vessels developed after partial embolization in 17.7% of patients. In the treatment completed group, this angiogenesis network completely resolved following total obliteration of the VGAM venous sac.23 DISCUSSION VGAMs are broadly classified into choroidal and mural types. The choroidal type is the most complex type, with multiple high-flow fistulas to the embryonic median vein of the prosencephalon and its choroidal venous tributaries, mainly located in the velum interpositum cistern medial to the choroidal fissure. The arterial feeders are from limbic system and are primarily the choroidal arcade, including anterior and posterior choroidal arteries, and the anterior cerebral arteries on either side through the pericallosal arcade. There is often additional supply from the quadrigeminal arteries and the thalamoperforators.4,5 These feeders are connected to each other and form artery to artery anastomosis before the fistulous points having moderate to extremely high flow. Their contribution evolves over time, and following partial treatment, as they become collaterals to resupply the fistulas, and can regress after closure of the high-flow shunt. The mural type of VGAMs is located either in the velum interpositum cistern or the quadrigeminal cistern. They consist of single or multiple fistulas into the median vein of prosencephalon, and usually are few, and fewer than the choroidal type. Quadrigeminal and/or posterior choroidal arteries often supply them. They typically have more round dilatation of the median vein of prosencephalon, which as it dilates may kink, restricting outflow, and may produce further dilatation of the aneurysmally dilated vein; that may then present as an acute macrocephaly, requiring urgent intervention.5 The VGAM formation is estimated to happen at embryonic stage of 21 to 23 mm (6 wk) and 50 mm (11 wk) of development.4 Genetic predisposition and association has been reported. RASA 1 mutation is an autosomal dominant disease causing capillary malformations (CM) and AVMs (CM-AVM syndrome). Recent review of 140 cases of RASA 1 mutation in 50 families showed 2 VGAMs.9 Heuchan et al10 found 4 RASA 1 mutations in 11 VGAM cases. Antenatal diagnosis occurred in 12 of our patients with VGAM following routine antenatal USG subsequently underwent antenatal MRI for more detailed evaluation, pediatric cardiology evaluation including fetal ultrasound and echocardiography. Maternal digoxin was administered before delivery and delivered in a controlled situation by either C-section or vaginal delivery. Neonates with CHF were managed medically in the intensive care unit by respiratory support with or without intubation, evaluated by echocardiogram, transcranial ultrasonogram, and subsequently MRI of the brain. Based on the clinical situation, anatomic type of VGAM and cardiac status including significant diastolic flow reversal in the descending aorta, a decision was made on urgent intervention. Past the neonatal period, most patients present with progressive hydrodynamic dysfunction, presenting as progressive enlargement of head circumference and hydrocephalus during infancy and early childhood (Table 3).11 It may rarely present as melting brain syndrome.25 During infancy and childhood, VGAM were diagnosed during evaluation for loss of achieved milestones, prominent, pulsatile facial veins, headache, seizures, and incidentally during evaluation for trauma, evaluation for congenital cardiac abnormality, etc. A number of our patients also had prominent facial and scalp veins as a complaint by the parents but we do not know if that is significant enough complaint to advise screening. Hydrodynamic disorder explains the pathophysiology of VGAM presentation in infancy and early childhood. The main absorption pathway of the CSF is the arachnoid granulations in the matured brain driven by the sump effect due to negative pressure in the dural sinuses. The high-flow shunts cause increased pressure in the venous sinus, resulting in CSF malabsorption. It is made worse by additional factors such as pulmonary hypertension if present, skull base maturation, and delayed maturation of the jugular bulb.12 This venous hypertension may produce a pseudo Chiari type tonsilar herniation, which is reversible with closure of the malformation. Ventriculomegaly can occur due to subependymal atrophy without increased intracranial pressure. Venous ischemia of the brain over time induces bilateral subcortical white matter calcification and atrophy of brain, which is manifested by psychomotor developmental delay, and seizures. If venous drainage of the VGAM refluxes from the dural sinus to the cortical vein, seizures and focal neurological deficits can develop, which are usually the symptoms of older children. Rarely, “Melting brain syndrome” can occur in fetuses, neonated, and less frequently in infants due to subacute progression of venous hypertension resulting in decreased cerebral blood flow and subacute progressive destruction of brain parenchyma. Again, here the ventricular system is enlarged without raised intracranial pressure. Obstructive hydrocephalus in VGAM is rare, although aqueduct of Sylvius compression by the VGAM sac may be present. Two-thirds of our patients had ventricular enlargement either during presentation or during the observation period. Our strategy was to treat the disease early by endovascular embolization to reduce hydrodynamic pressure and reserve CSF diversion procedure for refractory cases. Ventricular shunting reverses the pressure gradient from subarachnoid space to the superior sagittal sinus. Shunting can result in dilatation of the draining vein of the VGAM, calcification of the white matter, and subependymal atrophy. It can also result in subdural hygroma, hematomas, and slit ventricles.12 We had to resort to either ventriculoperitoneal shunting or endoscopic third ventriculostomy in only one-fourth of the patients being treated for hydrocephalus. Before endovascular embolization, we take into consideration the physical parameters and imaging features. The weight of the child, the head circumference, and its change over time are noted. We do MRI, magnetic resonance angiography (MRA), and magnetic resonance venography and look at enlarged feeders, venous dilatation, and venous sinus occlusion, status of the brain including encephalomalacia, atrophy, calcification, and size of the ventricles. In view of the information obtained from excellent noninvasive imaging, there is no role for doing only diagnostic angiography as it may damage femoral access needed for treatment.13 The treatment timing is decided on multiple factors that include growth and development of the child, progression of neurological symptoms, cardiac features, and imaging features. Early endovascular intervention is performed if the cardiac condition is unstable or progressive in spite of maximal medical treatment, progressive macrocrania or hydrocephalus, new onset developmental delay or milestone regression, and other imaging features including of venous ischemic changes such as calcifications. In clinically stable patients, it is preferable to delay treatment until 5 to 6 mo of the age. Patients with known VGAM since birth are advised to follow with pediatrician and/or pediatric neurologist at least once every 2 wk for assessment including head circumference, and noncontrast computed tomography (NCCT) of the head is advised at 4, 8, 16, and 24 wk looking for hydrocephalus, cerebral calcification, features of melting brain syndrome. Sometimes we alternate NCCT with MRI; CT is easily performed without anesthesia and readily gives information about the CSF spaces and calcifications, while MRI is more difficult to perform but more informative on the subtle changes in brain parenchyma. Treatment by endovascular embolization is the preferred method for this group of vascular malformation as surgical treatment had significant mortality.14 Our final goal is complete obliteration of the malformation with normal development without focal neurological deficits that is usually achieved in multiple stages. The immediate treatment goal of each stage of treatment depends on age and presentation. In neonates, the immediate goal is to alleviate CHF, in the infant and early childhood, it is to restore the normal hydrovenous equilibrium allowing normal development of the brain. At this age, aggressive endovascular embolization avoids ventricular shunting. Endovascular embolization performed after the development of established hydrocephalus may be insufficient, and third ventriculostomy or ventricular shunt may be needed. A total of 66.6% of our patients had hydrocephalus, which included 70% choroidal and 58% mural types. We treated almost all cases aggressively with embolization and only one-fourth (25%) needed CSF diversion procedure. In the treatment of VGAM, major breakthrough began in the early 1980s with the evolution of endovascular embolization.15-17 Lasjaunias et al18-20 reported complete transarterial occlusion and cure in 1989. Since then there has been major progress in endovascular treatment. We perform endovascular treatment of VGAM by transfemoral, transarterial embolization as our first choice for treatment. We take advantage of the general anesthesia for the procedure to do pretherapeutic MRI and MRA of the brain under same anesthesia. Transarterial embolization is done using a flow-guided microcatheter using high-concentration N-butyl-cyanoacrylate (n-BCA) mixed with contrast ethiodol and tantalum powder to increase radiopacity under systemic hypotension.21 We believe n-BCA is the ideal agent for high-flow fistula like other experienced operators.11,22,23 Coils are best avoided as it results in proximal occlusion fistula, later leading to development of collateral network of vessels without occluding the fistula. This makes further treatment difficult. Onyx is best reserved for embolization after the shunt flow through the VGAM is significantly reduced by the preceding n-BCA embolizations and it is the agent of choice in cases with dural recruitment. In most cases, multiple-staged embolization is needed. In our series, choroidal types required more sessions of embolization compared to mural type, 4.3 as against 2.9 procedures per patient. Rarely, complete obliteration in one is achieved in 1 session for a mural-type VGAM. Clinical symptoms usually improve after partial embolization, and staged embolization over several years are done to achieve complete obliteration. Treatment interval is determined based on clinical response, and in clinically stable patient, subsequent treatments are planned in 3 to 6-mo interval. Based on our experience, the transvenous approach is associated with a higher rate of postembolization hemorrhage compared to transarterial embolization as the dilated venous pouch of the VGAM can be connected to the subependymal vein via the choroidal vein, or other veins of the deep structures, with the underdeveloped internal cerebral vein. One of the mortalities in the current series happened due to excess glue penetration into the venous sac following transarterial embolization resulting in postprocedure thrombosis of the venous sac and extensive hemorrhage. One intracerebral hemorrhage in the current series is following transvenous embolization. We now reserve transvenous embolization for cases nearing the end of treatment with small residual shunt assuming the hemorrhagic risk is low. Dural feeders to the VGAM may be observed on initial or follow-up angiogram during staged embolization. Overall, it happens in about 30% of cases,24 and in the current series, it was noted in 22.2% of patients mostly into the dilated vein of Galen sac and rarely along the major venous sinuses. Dural shunting on the initial angiogram was observed in relatively old patients and was considered secondary development mainly due to nonsprouting angiogenesis due to the sump effect of high-flow shunting. De novo dural shunting during staged embolization can be due to sprouting or nonsprouting angiogenesis. Sprouting angiogenesis is induced by vascular endothelial growth factor or other angiogenic factors.24,25 Prognosis of this secondary dural shunting is unknown, but we favor embolization to prevent possible aggravation of venous hypertension. During the staged treatment by endovascular embolization, a new parenchymal angiogenetic network of vessels was seen in 17.7% of cases in our series. In treatment completed groups, this has completely resolved following total obliteration of the dilated venous sac. Stereotactic radiotherapy has a limited role in the treatment of VGAM. It may be useful in older patients after stages of endovascular embolization and left with relatively slow flow residual shunts. Only one of our patients in the current series underwent radiosurgery to achieve complete obliteration of the fistula. In our series of 113 patients, after exclusion based on the criterion mentioned earlier, we had 45 infants and older children. We achieved cure in 82.2% of patients, while 13.3% are still under treatment and had 4.5% mortality. Among them, 66.6% are neurologically and developmentally intact with an outcome score of 4. Nine patients (20%) had outcome score of 3 with mild impairment and 4 patients (8.9%) had outcome score of 2 with moderate impairment of function. Procedure-related complications happened in 11% of patients including 4 intracerebral hemorrhage, 1 stroke, and 1 subarachnoid hemorrhage. Spontaneous thrombosis of the enlarge vein of Galen venous pouch occurred in one of our cases at the time of angiography and are not included in this series, and has been rarely reported.26 Our follow-up protocol after complete or near-complete obliteration of VGAM is to perform follow-up angiography at 6 to 12 mo. Most cases with near-complete obliteration progressed to complete obliteration on follow-up. On angiographic confirmation of obliteration of the fistulas, MRI imaging is obtained after 3 to 5 yr. CONCLUSION Technical and technological advancements in endovascular embolization along with better understanding of the clinical, anatomic, and pathophysiological features have resulted in significantly improved outcome and prognosis in VGAM. Transarterial embolization is the primary treatment of choice targeted to obliterate the fistula site for effective embolization. Staged embolization is done in most cases to minimize the treatment risk. The majority of children with VGAM can now survive and most develop normally following appropriately timed treatment. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Sahs AL , Perret G , Locksley HB , Nishioka H , Skultety FM . Preliminary remarks on subarachnoid hemorrhage . J NeuroIntervent Surg . 1966 ; 24 ( 4 ): 321 – 326 . 2. Locksley HB . Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations . J Neurosurg . 1966 ; 25 ( 3 ): 321 – 368 . Google Scholar CrossRef Search ADS PubMed 3. Locksley HB , Sahs AL , Knowler L . Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section II. General survey of cases in the central registry and characteristics of the sample population . J Neurosurg . 1966 ; 24 ( 5 ): 922 – 932 . Google Scholar CrossRef Search ADS PubMed 4. Raybaud CA , Strother CM , Hald JK . Aneurysms of the vein of Galen: embryonic considerations and anatomical features relating to the pathogenesis of the malformation . Neuroradiology . 1989 ; 31 ( 2 ): 109 – 128 . Google Scholar CrossRef Search ADS PubMed 5. Berenstein A , Lasjaunias P . Arteriovenous fistulas of the brain . In: Surgical Neuroangiography 4 Endovascular Treatment of Cerebral Lesions . 1st ed . Berlin, Heidelberg : Springer-Verlag ; 1992 : 267 – 317 . 6. Garcia-Monaco R , Lasjaunias P , Berenstein A . Therapeutic management of vein of Galen aneurysmal malformations . In: Vinuela F , Halbach V , Dion J , eds. Interventional Neuroradiology: Endovascular Therapy of the Central Nervous System . New York : Raven Press ; 1992 : 113 – 127 . 7. Berenstein A , Fifi JT , Niimi Y et al. Vein of Galen malformations in neonates: new management paradigms for improving outcomes . Neurosurgery . 2012 ; 70 ( 5 ): 1207 – 1213 . Google Scholar CrossRef Search ADS PubMed 8. Jones BV , Ball WS , Tomsick TA , Millard J , Crone KR . Vein of Galen aneurysmal malformation: diagnosis and treatment of 13 children with extended clinical follow-up . AJNR Am J Neuroradiol . 2002 ; 23 ( 10 ): 1717 – 1724 . Google Scholar PubMed 9. Revencu N , Boon LM , Mulliken JB et al. Parkes Weber syndrome, vein of Galen aneurysmal malformation, and other fast-flow vascular anomalies are caused by RASA1 mutations . Hum Mutat . 2008 ; 29 ( 7 ): 959 – 965 . Google Scholar CrossRef Search ADS PubMed 10. Heuchan AM , Young D . Early colour Doppler duct diameter and symptomatic patent ductus arteriosus in a cyclo-oxygenase inhibitor naive population . Acta Paediatr . 2013 ; 102 ( 3 ): 254 – 257 . Google Scholar CrossRef Search ADS PubMed 11. Lasjaunias PL , Chng SM , Sachet M , Alvarez H , Rodesch G , Garcia-Monaco R . The management of vein of Galen aneurysmal malformations . Neurosurgery . 2006 ; 59 ( 5 Suppl 3 ): S184 – S194 . Google Scholar PubMed 12. Lasjaunias P , Ter Brugge K , Berenstein A . Introduction and general comments regarding pediatric intracranial arteriovenous shunts . In: Surgical Neuroangiography 3 Clinical and Inteventional Aspects in Children . 2nd ed . Berlin, Heidelberg : Springer ; 2006 : 27 – 104 . Google Scholar CrossRef Search ADS 13. Berenstein A , Niimi Y , Song J , Lasjaunias P . Vein of galen aneurysmal malformation . In: Albright A , Pollack I , Adelson P , eds. Principles and Practice of Pediatric Neurosurgery , 2nd ed . New York : Thieme ; 2008 : 1014 – 1028 . Google Scholar CrossRef Search ADS 14. Khullar D , Andeejani AM , Bulsara KR . Evolution of treatment options for vein of Galen malformations . J Neurosurg Pediatr . 2010 ; 6 ( 5 ): 444 – 451 . Google Scholar CrossRef Search ADS PubMed 15. Berenstein A , Krischeff II . Catheter and material selection for transarterial embolization: technical considerations. I. Catheters . Radiology . 1979 ; 132 ( 3 ): 619 – 630 . Google Scholar CrossRef Search ADS PubMed 16. Berenstein A , Kricheff II . Microembolization techniques of vascular occlusion: radiologic, pathologic, and clinical correlation . AJNR Am J Neuroradiol . 1981 ; 2 ( 3 ): 261 – 267 . Google Scholar PubMed 17. Berenstein A , Kricheff II . Catheter and material selection for transarterial embolization: technical considerations. II. Materials . Radiology . 1979 ; 132 ( 3 ): 631 – 639 . Google Scholar CrossRef Search ADS PubMed 18. Lasjaunias P . Vein of Galen malformations . Neurosurgery . 1989 ; 25 ( 4 ): 666 – 667 . Google Scholar CrossRef Search ADS PubMed 19. Lasjaunias P , Rodesch G , Pruvost P , Laroche FG , Landrieu P . Treatment of vein of Galen aneurysmal malformation . J Neurosurg . 1989 ; 70 ( 5 ): 746 – 750 . Google Scholar CrossRef Search ADS PubMed 20. Lasjaunias P , Rodesch G , Terbrugge K et al. Vein of Galen aneurysmal malformations. Report of 36 cases managed between 1982 and 1988 . Acta Neurochir . 1989 ; 99 ( 1-2 ): 26 – 37 . Google Scholar CrossRef Search ADS PubMed 21. Berenstein A , Niimi Y , Song J , Lasjaunias P . Vein of Galen aneurysmal malformation . In: Albright A , Pollack I , Adelson P , eds. Principles and Practice of Pediatric Neurosurgery , 2nd ed . New York : Thieme ; 2008 : 1014 – 1028 . Google Scholar CrossRef Search ADS 22. Hoang S , Choudhri O , Edwards M , Guzman R . Vein of Galen malformation . Neurosurg Focus . 2009 ; 27 ( 5 ): E8 . Google Scholar CrossRef Search ADS PubMed 23. Gailloud P , O’Riordan DP , Burger I et al. Diagnosis and management of vein of galen aneurysmal malformations . J Perinatol . 2005 ; 25 ( 8 ): 542 – 51 . Google Scholar CrossRef Search ADS PubMed 24. Paramasivam S , Niimi Y , Meila D , Berenstein A . Dural arteriovenous shunt development in patients with vein of galen malformation . Interv Neuroradiol . 2014 ; 20 ( 6 ): 781 – 790 . Google Scholar CrossRef Search ADS PubMed 25. Paramasivam S , Toma N , Niimi Y , Berenstein A . De novo development of dural arteriovenous fistula after endovascular embolization of pial arteriovenous fistula . J Neurointerv Surg . 2013 ; 5 ( 4 ): 321 – 326 . Google Scholar CrossRef Search ADS PubMed 26. Rodesch G , Lasjaunias P , Terbrugge K , Burrows P . Intracranial arteriovenous vascular lesions in children. Role of endovascular technics apropos of 44 cases . Neurochirurgie . 1988 ; 34 ( 5 ): 293 – 303 . Google Scholar PubMed Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Neurosurgery Oxford University Press

Vein of Galen Aneurysmal Malformation: Advances in Management and Endovascular treatment

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Congress of Neurological Surgeons
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Copyright © 2018 by the Congress of Neurological Surgeons
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0148-396X
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1524-4040
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10.1093/neuros/nyy100
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Abstract

Abstract BACKGROUND Vein of Galen aneurysmal malformation (VGAM) is a rare congenital vascular malformation representing <1% of all arteriovenous malformations. The knowledge and strategies in the management are constantly evolving. OBJECTIVE To review our series of postneonatal VGAM patients treated over 11-yr period. METHODS Retrospective analysis of 113 VGAM treated between January 2004 and April 2015. After exclusions, 45 patients were included: 33 choroidal and 12 mural types. RESULTS Presenting symptom in the order of frequency: enlarged head circumference, antenatal diagnosis, mild CHF, and PHT at birth. Older patients were diagnosed following trauma, headache, cognitive decline, and incidentally during workup for other diseases. Hydrocephalus due to hydrodynamic disorder was present in 70% of choroidal and 58% of mural types. Only a quarter needed cerebrospinal fluid diversion procedure. Radiological cure was achieved in 82%; the outcome graded on a 5-point scale: 0 (death) to 4 (normal). A total of 66.6% are neurologically and developmentally intact with outcome score 4, 20% had outcome score of 3, and 8.9% had outcome score of 2. There was 4.4% mortality. Dural feeders to VGAM were found either in the initial or during the treatment in 22.2% in the current series. Angiogenesis from pial vessels developed after partial embolization in 17.7% that resolved completely following complete obliteration of VGAM. CONCLUSION Technical and technological advancements in endovascular embolization along with better understanding of clinical, anatomic, and pathophysiological aspects have resulted in significantly improved outcome and prognosis in VGAM. Most patients with proper treatment can now survive and most develop normally following appropriately timed treatment. Vein of Galen, AV Malformation, AV fistula, Endovascular embolization ABBREVIATIONS ABBREVIATIONS AVM arteriovenous malformation CHF congestive heart failure CM capillary malformation CSF cerebrospinal fluid DSA digital subtraction angiography ICA internal carotid artery MRA magnetic resonance angiography MRI magnetic resonance imaging n-BCA N-butyl-cyanoacrylate NCCT noncontrast computed tomography PHT pulmonary hypertension USG ultrasonogram VGAD vein of Galen aneurysmal dilatation VGAM vein of Galen aneurysmal malformation Vein of Galen aneurysmal malformation (VGAM) is a rare congenital vascular disorder representing less than 1% of all arteriovenous malformations (AVMs) in the cooperative study of subarachnoid hemorrhage.1-3 The exact incidence is difficult to determine, as there is significant diagnostic confusion among various malformations that cause dilatation of the vein of Galen or its embryonic precursor. VGAM is located in the subarachnoid space in the choroid fissure and embryologically related to the development of the choroid plexus as demonstrated by Raybaund et al in 1989.4 The concept of this disease was further elucidated by Berenstein et al5 and Garcia-Monaco et al,6 who defined VGAM as arteriovenous fistulas draining to the embryonic precursor of the vein of Galen called median vein of prosencephalon. These studies subclassified VGAM further into choroidal and the mural types. Other vascular lesions including pial or dural arteriovenous malformation that cause dilatation of the “true” (embryologically matured) vein of Galen were designated as vein of Galen aneurysmal dilatation (VGAD). Vein of Galen varix is a dilated vein of Galen without arteriovenous shunts.5 The knowledge and strategies in the management of VGAM are constantly evolving. We reviewed our series of postneonatal VGAM patients treated over an 11-yr period and have discussed the presentation, management strategies, results, and clinical outcome. METHODS We retrospectively reviewed the patients with dilated vein of Galen treated at our center between January 2004 and April 2015. Appropriate institutional review board approval was obtained for retrospective review of the nonidentifiable patient information and appropriate patient consent obtained. We categorized them as VGAM of either choroidal or mural types and VGAD. We also categorized them based on the timing of treatment as neonatal and older. For the study purpose we excluded, VGAM treated partly before 2004, VGAM treated at outside institution before we took over the care, VGAD, and VGAM treated in the neonatal period were excluded, as we have reported them previously.7 We gathered clinical information and procedure details from the patient chart, reviewed the images for categorization and analysis of outcome. The referring physician and/or the patient family was called to find the current functional activity using a standardized age appropriate questionnaire. They were then graded on a 5-point scale suggested by Jones et al,8 ranging from 0 (death) to 4 (normal). Children having severe neurological impairment, requiring intensive supportive care and medical management were given a score of 1. Presence of moderate neurological impairment affecting activities of daily living and requiring significant support in educational and social interactions but a lesser degree of daily medical management were given a score of 2. Children who had milder degree of impairment, resulting in some need for social and educational support, with medical management only on occasion were a given score of 3.8 RESULTS In total, we reviewed 113 patients with enlarged vein of Galen treated at our center between January 2004 and April 2015. We excluded 23 patients with treatment initiated before 2004 as we did not have the complete set of images for review. We excluded 14 patients initially treated at outside institution as the initial management strategy was different from ours and most of them were referred following a clinical complication. We excluded the VGAM treated in the neonatal period (21 patients) as we have published a series previously.7 We also excluded 10 patients with VGAD that will be reported separately. After exclusion, we had a subset of 45 patients of VGAM that presented to and treated by our team from the beginning (Table 1). TABLE 1. Overview of Our Series of Cases Treated Between January 2004 and April 2015 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 View Large TABLE 1. Overview of Our Series of Cases Treated Between January 2004 and April 2015 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 Total Cases 113 Treatment initiated before 2004 23 Pretreated at other institutions 14 Treated in the neonatal period 21 VOGAD 10 VOGM 45 View Large Of the 45 patients selected for the analysis, 33 were choroidal and 12 were mural type. Among 33 choroidal VGAM, M:F ratio was 17:16, and among the 12 mural VGAM, M:F ratio was 7:5. The most common presenting symptom was progressive increased head circumference and antenatal diagnosis with scans followed by mild congestive heart failure and pulmonary hypertension at birth that was managed medically. Other patients were diagnosed following scans done for trauma to head, and others presented with headache, cognitive decline, and incidentally during workup for other diseases (Table 2). TABLE 2. Clinical Presentation of Each of Our Cases Along With Segregation Into the Choroidal and Mural types of VGAM S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 View Large TABLE 2. Clinical Presentation of Each of Our Cases Along With Segregation Into the Choroidal and Mural types of VGAM S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 S. No Presentation Overall Choroidal Mural 1 Increased head circumference 13 10 3 2 Diagnosed in utero 12 7 5 3 CHF and PHT at birth 6 5 1 4 Trauma 4 3 1 5 Pulsating prominent facial vein 3 2 1 6 Headache 2 2 0 7 Cognitive decline 1 1 0 8 Cardiac abnormality— SOB/failure to thrive 1 0 1 9 Seizures at birth 1 1 0 10 Seizures 1 1 0 11 Incidental—craniosynostosis 1 1 0 Total 45 33 12 View Large Analyzing the timing of diagnosis, a significant number of patients were diagnosed antenatally with USG followed by fetal magnetic resonance imaging (MRI), but majority of patients in the study group were diagnosed in neonatal, infancy, and early childhood (Table 3). In our series, all mural and most choroidal VGAM were diagnosed before 12 mo of age. All the patients selected for the analysis here were either stable or managed medically in the neonatal period. Based on our protocol, the VGAM known since birth were periodically followed both clinically and radiologically till 6 mo of age when definitive treatment was initiated. Most of our patients were treated during infancy as planned (Table 3). However, in the subgroup analysis among the 6 patients presenting with CHF and PHT in the neonatal period that were managed medically, 5 developed hydrovenous dysfunction before 6 mo of age and were treated by endovascular embolization, while among the 12 patients diagnosed antenatally and were born without CHF, only 3 patients needed endovascular embolization earlier than 6 mo. TABLE 3. The Data Depicts the Time of Clinical Presentation and the Timing of Treatment in Choroidal and Mural-Type VGAM Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 View Large TABLE 3. The Data Depicts the Time of Clinical Presentation and the Timing of Treatment in Choroidal and Mural-Type VGAM Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 Age at Presentation Age at first Treatment Choroidal Antenatal 7 0-1 mo 10 1-12 mo 11 24 1-5 yr 3 7 >5 yr 2 2 Total 33 33 Mural Antenatal 5 0-1 mo 2 1-12 mo 5 9 1-5 yr 2 >5 yr 1 Total 12 12 View Large Hydrocephalus due to hydrodynamic disorder manifested as ventricular and cerebrospinal fluid (CSF) space enlargement associated with VGAM is common. In the current series, 23 out of 33 patients with choroidal type (70%) had hydrodynamic hydrocephalus. Only 6 of them underwent venriculoperitoneal shunt placement and 2 had endoscopic third ventriculostomy. Seven of 12 patients with mural type of VGAM had hydrocephalus (58%). None of these patients were treated by CSF diversion procedure. Overall, two-thirds (66.6%) of the patients presented with hydrocephalus and among them only one-fourth of them (26.6%) needed special procedure for CSF diversion, rest of the patients were managed by reducing the hydrovenous pressure by embolization. Among the 45 patients, in 37 (82%) we achieved radiological cure of the malformation and 6 patients (13.3%) are still under treatment (Table 4). To achieve this cure, choroidal VGAM (Figures 1 and 2) had between 2 and 11 procedures per patient with an average of 4.3 procedures, while mural VGAM (Figure 3) had between 1 and 8 procedures per patient with an average of 2.9 procedures per patient. FIGURE 1. View largeDownload slide Child born of a full-term normal delivery presented with prominent facial veins along with macrocephaly and developmental regression. A-D, At 10 mo of age he was diagnosed with VGAM. Brain CT and MRI show the enlarged vein of Galen (A and B) and its enlarged choroidal feeding vessels (C and D). E and F, Digital subtraction angiography (DSA) of left vertebral artery reveals enlarged bilateral posterolateral choroidal arteries feeding the VGAM. G and H, DSA of left internal carotid artery (ICA) reveals an enlarged anterior choroidal artery supplying the VGAM, and the venous phase shows narrowing of the falcine sinus and nonmaturation of jugular bulb on either side. I and J, DSA of the right ICA reveals additional supply through enlarged anterior cerebral artery into the enlarged remnant of median vein of procencephalon constituting the malformation. K and L, Superselective microcatheter angiogram through the left anterior choroidal artery reveals the enlarged feeder, large fistula opening into the malformation. FIGURE 1. View largeDownload slide Child born of a full-term normal delivery presented with prominent facial veins along with macrocephaly and developmental regression. A-D, At 10 mo of age he was diagnosed with VGAM. Brain CT and MRI show the enlarged vein of Galen (A and B) and its enlarged choroidal feeding vessels (C and D). E and F, Digital subtraction angiography (DSA) of left vertebral artery reveals enlarged bilateral posterolateral choroidal arteries feeding the VGAM. G and H, DSA of left internal carotid artery (ICA) reveals an enlarged anterior choroidal artery supplying the VGAM, and the venous phase shows narrowing of the falcine sinus and nonmaturation of jugular bulb on either side. I and J, DSA of the right ICA reveals additional supply through enlarged anterior cerebral artery into the enlarged remnant of median vein of procencephalon constituting the malformation. K and L, Superselective microcatheter angiogram through the left anterior choroidal artery reveals the enlarged feeder, large fistula opening into the malformation. FIGURE 2. View largeDownload slide View largeDownload slide (Continuation of the images from Figure 1). A and B, Superselective microcatheter angiogram through the anterior cerebral artery reveals another large feeder draining into the malformation. C, Glue cast at the end of first embolization session. D, The residual shunt is shown with right ICA angiogram at the end of first embolization session. E and F, Six months later second procedure was performed, the residual shunt is seen. Further embolization of few pedicles from right and left posterolateral choroidal arteries was performed. G and H, At the end of second embolization procedure, the flow to the malformation was significantly reduced with good blood flow to the brain tissue. I-N, Six-month follow-up angiograms of the right ICA, left ICA, and left vertebral artery reveal complete obliteration of the VGAM. O and P, MRI brain reveals complete obliteration, and normal development of the brain and MRA show the normal vasculature. FIGURE 2. View largeDownload slide View largeDownload slide (Continuation of the images from Figure 1). A and B, Superselective microcatheter angiogram through the anterior cerebral artery reveals another large feeder draining into the malformation. C, Glue cast at the end of first embolization session. D, The residual shunt is shown with right ICA angiogram at the end of first embolization session. E and F, Six months later second procedure was performed, the residual shunt is seen. Further embolization of few pedicles from right and left posterolateral choroidal arteries was performed. G and H, At the end of second embolization procedure, the flow to the malformation was significantly reduced with good blood flow to the brain tissue. I-N, Six-month follow-up angiograms of the right ICA, left ICA, and left vertebral artery reveal complete obliteration of the VGAM. O and P, MRI brain reveals complete obliteration, and normal development of the brain and MRA show the normal vasculature. FIGURE 3. View largeDownload slide View largeDownload slide Child born of a full-term normal delivery developed increased head circumference and prominent facial and scalp veins at 7 mo of age. Evaluation with CT scan brain (A) and MRI brain (B) reveals VGAM with significantly enlarged ventricular system. C, Prominent facial and scalp veins. DSA examination of left vertebral artery (D) and (E), right ICA (F–H), and left ICA (I) and (J) reveals a mural type of VGAM. The images also reveal that the vein of Galen sac is significantly enlarged with narrowing of falcine sinus and enlargement of superior sagittal sinus. There is also dysmaturation of the jugular bulb resulting in collateral venous drainage along scalp and facial veins. H, Collateral venous drainage following right ICA angiogram. K and L, Microcatheterization and superselective angiogram reveal a single-hole high-flow fistula. M and N, Glue case for glue injection under systemic hypotension. O and P, Immediate postembolization angiogram reveals complete obliteration of the malformation. The child head circumference stabilized and the enlarged facial and scalp veins became less prominent over time and the child achieved normal developmental milestones. Q-T, Six-month follow-up angiogram reveals persistent complete obliteration of the malformation. U, Follow-up CT brain reveals normal development of the brain with stable ventricular size. FIGURE 3. View largeDownload slide View largeDownload slide Child born of a full-term normal delivery developed increased head circumference and prominent facial and scalp veins at 7 mo of age. Evaluation with CT scan brain (A) and MRI brain (B) reveals VGAM with significantly enlarged ventricular system. C, Prominent facial and scalp veins. DSA examination of left vertebral artery (D) and (E), right ICA (F–H), and left ICA (I) and (J) reveals a mural type of VGAM. The images also reveal that the vein of Galen sac is significantly enlarged with narrowing of falcine sinus and enlargement of superior sagittal sinus. There is also dysmaturation of the jugular bulb resulting in collateral venous drainage along scalp and facial veins. H, Collateral venous drainage following right ICA angiogram. K and L, Microcatheterization and superselective angiogram reveal a single-hole high-flow fistula. M and N, Glue case for glue injection under systemic hypotension. O and P, Immediate postembolization angiogram reveals complete obliteration of the malformation. The child head circumference stabilized and the enlarged facial and scalp veins became less prominent over time and the child achieved normal developmental milestones. Q-T, Six-month follow-up angiogram reveals persistent complete obliteration of the malformation. U, Follow-up CT brain reveals normal development of the brain with stable ventricular size. TABLE 4. The Overall Outcome of Treatment in Choroidal and Mural Types are Represented. The Cure Mentioned Here Means the Angiographic Cure Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 View Large TABLE 4. The Overall Outcome of Treatment in Choroidal and Mural Types are Represented. The Cure Mentioned Here Means the Angiographic Cure Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 Result or Embolization Chroidal Mural Cure 27(81%) 10(83%) In treatment 4 2 Death 2 0 Total 33 12 View Large In the 45 patients with VGAM, there were 2 deaths (4.4% mortality). Among the rest that include radiologically cured and patients still undergoing treatment in stages, 30 patients (66.6%) were neurologically and developmentally intact with an outcome score of 4. Nine patients (20%) had outcome score of 3 with mild impairment, and 4 patients (8.9%) had outcome score of 2 with moderate impairment of function. Dural feeders to the VGAM were found either initially or during the course of treatment in 22.2% of patients in the current series. Angiogenesis from pial vessels developed after partial embolization in 17.7% of patients. In the treatment completed group, this angiogenesis network completely resolved following total obliteration of the VGAM venous sac.23 DISCUSSION VGAMs are broadly classified into choroidal and mural types. The choroidal type is the most complex type, with multiple high-flow fistulas to the embryonic median vein of the prosencephalon and its choroidal venous tributaries, mainly located in the velum interpositum cistern medial to the choroidal fissure. The arterial feeders are from limbic system and are primarily the choroidal arcade, including anterior and posterior choroidal arteries, and the anterior cerebral arteries on either side through the pericallosal arcade. There is often additional supply from the quadrigeminal arteries and the thalamoperforators.4,5 These feeders are connected to each other and form artery to artery anastomosis before the fistulous points having moderate to extremely high flow. Their contribution evolves over time, and following partial treatment, as they become collaterals to resupply the fistulas, and can regress after closure of the high-flow shunt. The mural type of VGAMs is located either in the velum interpositum cistern or the quadrigeminal cistern. They consist of single or multiple fistulas into the median vein of prosencephalon, and usually are few, and fewer than the choroidal type. Quadrigeminal and/or posterior choroidal arteries often supply them. They typically have more round dilatation of the median vein of prosencephalon, which as it dilates may kink, restricting outflow, and may produce further dilatation of the aneurysmally dilated vein; that may then present as an acute macrocephaly, requiring urgent intervention.5 The VGAM formation is estimated to happen at embryonic stage of 21 to 23 mm (6 wk) and 50 mm (11 wk) of development.4 Genetic predisposition and association has been reported. RASA 1 mutation is an autosomal dominant disease causing capillary malformations (CM) and AVMs (CM-AVM syndrome). Recent review of 140 cases of RASA 1 mutation in 50 families showed 2 VGAMs.9 Heuchan et al10 found 4 RASA 1 mutations in 11 VGAM cases. Antenatal diagnosis occurred in 12 of our patients with VGAM following routine antenatal USG subsequently underwent antenatal MRI for more detailed evaluation, pediatric cardiology evaluation including fetal ultrasound and echocardiography. Maternal digoxin was administered before delivery and delivered in a controlled situation by either C-section or vaginal delivery. Neonates with CHF were managed medically in the intensive care unit by respiratory support with or without intubation, evaluated by echocardiogram, transcranial ultrasonogram, and subsequently MRI of the brain. Based on the clinical situation, anatomic type of VGAM and cardiac status including significant diastolic flow reversal in the descending aorta, a decision was made on urgent intervention. Past the neonatal period, most patients present with progressive hydrodynamic dysfunction, presenting as progressive enlargement of head circumference and hydrocephalus during infancy and early childhood (Table 3).11 It may rarely present as melting brain syndrome.25 During infancy and childhood, VGAM were diagnosed during evaluation for loss of achieved milestones, prominent, pulsatile facial veins, headache, seizures, and incidentally during evaluation for trauma, evaluation for congenital cardiac abnormality, etc. A number of our patients also had prominent facial and scalp veins as a complaint by the parents but we do not know if that is significant enough complaint to advise screening. Hydrodynamic disorder explains the pathophysiology of VGAM presentation in infancy and early childhood. The main absorption pathway of the CSF is the arachnoid granulations in the matured brain driven by the sump effect due to negative pressure in the dural sinuses. The high-flow shunts cause increased pressure in the venous sinus, resulting in CSF malabsorption. It is made worse by additional factors such as pulmonary hypertension if present, skull base maturation, and delayed maturation of the jugular bulb.12 This venous hypertension may produce a pseudo Chiari type tonsilar herniation, which is reversible with closure of the malformation. Ventriculomegaly can occur due to subependymal atrophy without increased intracranial pressure. Venous ischemia of the brain over time induces bilateral subcortical white matter calcification and atrophy of brain, which is manifested by psychomotor developmental delay, and seizures. If venous drainage of the VGAM refluxes from the dural sinus to the cortical vein, seizures and focal neurological deficits can develop, which are usually the symptoms of older children. Rarely, “Melting brain syndrome” can occur in fetuses, neonated, and less frequently in infants due to subacute progression of venous hypertension resulting in decreased cerebral blood flow and subacute progressive destruction of brain parenchyma. Again, here the ventricular system is enlarged without raised intracranial pressure. Obstructive hydrocephalus in VGAM is rare, although aqueduct of Sylvius compression by the VGAM sac may be present. Two-thirds of our patients had ventricular enlargement either during presentation or during the observation period. Our strategy was to treat the disease early by endovascular embolization to reduce hydrodynamic pressure and reserve CSF diversion procedure for refractory cases. Ventricular shunting reverses the pressure gradient from subarachnoid space to the superior sagittal sinus. Shunting can result in dilatation of the draining vein of the VGAM, calcification of the white matter, and subependymal atrophy. It can also result in subdural hygroma, hematomas, and slit ventricles.12 We had to resort to either ventriculoperitoneal shunting or endoscopic third ventriculostomy in only one-fourth of the patients being treated for hydrocephalus. Before endovascular embolization, we take into consideration the physical parameters and imaging features. The weight of the child, the head circumference, and its change over time are noted. We do MRI, magnetic resonance angiography (MRA), and magnetic resonance venography and look at enlarged feeders, venous dilatation, and venous sinus occlusion, status of the brain including encephalomalacia, atrophy, calcification, and size of the ventricles. In view of the information obtained from excellent noninvasive imaging, there is no role for doing only diagnostic angiography as it may damage femoral access needed for treatment.13 The treatment timing is decided on multiple factors that include growth and development of the child, progression of neurological symptoms, cardiac features, and imaging features. Early endovascular intervention is performed if the cardiac condition is unstable or progressive in spite of maximal medical treatment, progressive macrocrania or hydrocephalus, new onset developmental delay or milestone regression, and other imaging features including of venous ischemic changes such as calcifications. In clinically stable patients, it is preferable to delay treatment until 5 to 6 mo of the age. Patients with known VGAM since birth are advised to follow with pediatrician and/or pediatric neurologist at least once every 2 wk for assessment including head circumference, and noncontrast computed tomography (NCCT) of the head is advised at 4, 8, 16, and 24 wk looking for hydrocephalus, cerebral calcification, features of melting brain syndrome. Sometimes we alternate NCCT with MRI; CT is easily performed without anesthesia and readily gives information about the CSF spaces and calcifications, while MRI is more difficult to perform but more informative on the subtle changes in brain parenchyma. Treatment by endovascular embolization is the preferred method for this group of vascular malformation as surgical treatment had significant mortality.14 Our final goal is complete obliteration of the malformation with normal development without focal neurological deficits that is usually achieved in multiple stages. The immediate treatment goal of each stage of treatment depends on age and presentation. In neonates, the immediate goal is to alleviate CHF, in the infant and early childhood, it is to restore the normal hydrovenous equilibrium allowing normal development of the brain. At this age, aggressive endovascular embolization avoids ventricular shunting. Endovascular embolization performed after the development of established hydrocephalus may be insufficient, and third ventriculostomy or ventricular shunt may be needed. A total of 66.6% of our patients had hydrocephalus, which included 70% choroidal and 58% mural types. We treated almost all cases aggressively with embolization and only one-fourth (25%) needed CSF diversion procedure. In the treatment of VGAM, major breakthrough began in the early 1980s with the evolution of endovascular embolization.15-17 Lasjaunias et al18-20 reported complete transarterial occlusion and cure in 1989. Since then there has been major progress in endovascular treatment. We perform endovascular treatment of VGAM by transfemoral, transarterial embolization as our first choice for treatment. We take advantage of the general anesthesia for the procedure to do pretherapeutic MRI and MRA of the brain under same anesthesia. Transarterial embolization is done using a flow-guided microcatheter using high-concentration N-butyl-cyanoacrylate (n-BCA) mixed with contrast ethiodol and tantalum powder to increase radiopacity under systemic hypotension.21 We believe n-BCA is the ideal agent for high-flow fistula like other experienced operators.11,22,23 Coils are best avoided as it results in proximal occlusion fistula, later leading to development of collateral network of vessels without occluding the fistula. This makes further treatment difficult. Onyx is best reserved for embolization after the shunt flow through the VGAM is significantly reduced by the preceding n-BCA embolizations and it is the agent of choice in cases with dural recruitment. In most cases, multiple-staged embolization is needed. In our series, choroidal types required more sessions of embolization compared to mural type, 4.3 as against 2.9 procedures per patient. Rarely, complete obliteration in one is achieved in 1 session for a mural-type VGAM. Clinical symptoms usually improve after partial embolization, and staged embolization over several years are done to achieve complete obliteration. Treatment interval is determined based on clinical response, and in clinically stable patient, subsequent treatments are planned in 3 to 6-mo interval. Based on our experience, the transvenous approach is associated with a higher rate of postembolization hemorrhage compared to transarterial embolization as the dilated venous pouch of the VGAM can be connected to the subependymal vein via the choroidal vein, or other veins of the deep structures, with the underdeveloped internal cerebral vein. One of the mortalities in the current series happened due to excess glue penetration into the venous sac following transarterial embolization resulting in postprocedure thrombosis of the venous sac and extensive hemorrhage. One intracerebral hemorrhage in the current series is following transvenous embolization. We now reserve transvenous embolization for cases nearing the end of treatment with small residual shunt assuming the hemorrhagic risk is low. Dural feeders to the VGAM may be observed on initial or follow-up angiogram during staged embolization. Overall, it happens in about 30% of cases,24 and in the current series, it was noted in 22.2% of patients mostly into the dilated vein of Galen sac and rarely along the major venous sinuses. Dural shunting on the initial angiogram was observed in relatively old patients and was considered secondary development mainly due to nonsprouting angiogenesis due to the sump effect of high-flow shunting. De novo dural shunting during staged embolization can be due to sprouting or nonsprouting angiogenesis. Sprouting angiogenesis is induced by vascular endothelial growth factor or other angiogenic factors.24,25 Prognosis of this secondary dural shunting is unknown, but we favor embolization to prevent possible aggravation of venous hypertension. During the staged treatment by endovascular embolization, a new parenchymal angiogenetic network of vessels was seen in 17.7% of cases in our series. In treatment completed groups, this has completely resolved following total obliteration of the dilated venous sac. Stereotactic radiotherapy has a limited role in the treatment of VGAM. It may be useful in older patients after stages of endovascular embolization and left with relatively slow flow residual shunts. Only one of our patients in the current series underwent radiosurgery to achieve complete obliteration of the fistula. In our series of 113 patients, after exclusion based on the criterion mentioned earlier, we had 45 infants and older children. We achieved cure in 82.2% of patients, while 13.3% are still under treatment and had 4.5% mortality. Among them, 66.6% are neurologically and developmentally intact with an outcome score of 4. Nine patients (20%) had outcome score of 3 with mild impairment and 4 patients (8.9%) had outcome score of 2 with moderate impairment of function. Procedure-related complications happened in 11% of patients including 4 intracerebral hemorrhage, 1 stroke, and 1 subarachnoid hemorrhage. Spontaneous thrombosis of the enlarge vein of Galen venous pouch occurred in one of our cases at the time of angiography and are not included in this series, and has been rarely reported.26 Our follow-up protocol after complete or near-complete obliteration of VGAM is to perform follow-up angiography at 6 to 12 mo. Most cases with near-complete obliteration progressed to complete obliteration on follow-up. On angiographic confirmation of obliteration of the fistulas, MRI imaging is obtained after 3 to 5 yr. CONCLUSION Technical and technological advancements in endovascular embolization along with better understanding of the clinical, anatomic, and pathophysiological features have resulted in significantly improved outcome and prognosis in VGAM. Transarterial embolization is the primary treatment of choice targeted to obliterate the fistula site for effective embolization. Staged embolization is done in most cases to minimize the treatment risk. The majority of children with VGAM can now survive and most develop normally following appropriately timed treatment. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Sahs AL , Perret G , Locksley HB , Nishioka H , Skultety FM . Preliminary remarks on subarachnoid hemorrhage . J NeuroIntervent Surg . 1966 ; 24 ( 4 ): 321 – 326 . 2. Locksley HB . Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations . J Neurosurg . 1966 ; 25 ( 3 ): 321 – 368 . Google Scholar CrossRef Search ADS PubMed 3. Locksley HB , Sahs AL , Knowler L . Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section II. General survey of cases in the central registry and characteristics of the sample population . J Neurosurg . 1966 ; 24 ( 5 ): 922 – 932 . Google Scholar CrossRef Search ADS PubMed 4. Raybaud CA , Strother CM , Hald JK . Aneurysms of the vein of Galen: embryonic considerations and anatomical features relating to the pathogenesis of the malformation . Neuroradiology . 1989 ; 31 ( 2 ): 109 – 128 . Google Scholar CrossRef Search ADS PubMed 5. Berenstein A , Lasjaunias P . Arteriovenous fistulas of the brain . In: Surgical Neuroangiography 4 Endovascular Treatment of Cerebral Lesions . 1st ed . Berlin, Heidelberg : Springer-Verlag ; 1992 : 267 – 317 . 6. Garcia-Monaco R , Lasjaunias P , Berenstein A . Therapeutic management of vein of Galen aneurysmal malformations . In: Vinuela F , Halbach V , Dion J , eds. Interventional Neuroradiology: Endovascular Therapy of the Central Nervous System . New York : Raven Press ; 1992 : 113 – 127 . 7. Berenstein A , Fifi JT , Niimi Y et al. Vein of Galen malformations in neonates: new management paradigms for improving outcomes . Neurosurgery . 2012 ; 70 ( 5 ): 1207 – 1213 . Google Scholar CrossRef Search ADS PubMed 8. Jones BV , Ball WS , Tomsick TA , Millard J , Crone KR . Vein of Galen aneurysmal malformation: diagnosis and treatment of 13 children with extended clinical follow-up . AJNR Am J Neuroradiol . 2002 ; 23 ( 10 ): 1717 – 1724 . Google Scholar PubMed 9. Revencu N , Boon LM , Mulliken JB et al. Parkes Weber syndrome, vein of Galen aneurysmal malformation, and other fast-flow vascular anomalies are caused by RASA1 mutations . Hum Mutat . 2008 ; 29 ( 7 ): 959 – 965 . Google Scholar CrossRef Search ADS PubMed 10. Heuchan AM , Young D . Early colour Doppler duct diameter and symptomatic patent ductus arteriosus in a cyclo-oxygenase inhibitor naive population . Acta Paediatr . 2013 ; 102 ( 3 ): 254 – 257 . Google Scholar CrossRef Search ADS PubMed 11. Lasjaunias PL , Chng SM , Sachet M , Alvarez H , Rodesch G , Garcia-Monaco R . The management of vein of Galen aneurysmal malformations . Neurosurgery . 2006 ; 59 ( 5 Suppl 3 ): S184 – S194 . Google Scholar PubMed 12. Lasjaunias P , Ter Brugge K , Berenstein A . Introduction and general comments regarding pediatric intracranial arteriovenous shunts . In: Surgical Neuroangiography 3 Clinical and Inteventional Aspects in Children . 2nd ed . Berlin, Heidelberg : Springer ; 2006 : 27 – 104 . Google Scholar CrossRef Search ADS 13. Berenstein A , Niimi Y , Song J , Lasjaunias P . Vein of galen aneurysmal malformation . In: Albright A , Pollack I , Adelson P , eds. Principles and Practice of Pediatric Neurosurgery , 2nd ed . New York : Thieme ; 2008 : 1014 – 1028 . Google Scholar CrossRef Search ADS 14. Khullar D , Andeejani AM , Bulsara KR . Evolution of treatment options for vein of Galen malformations . J Neurosurg Pediatr . 2010 ; 6 ( 5 ): 444 – 451 . Google Scholar CrossRef Search ADS PubMed 15. Berenstein A , Krischeff II . Catheter and material selection for transarterial embolization: technical considerations. I. Catheters . Radiology . 1979 ; 132 ( 3 ): 619 – 630 . Google Scholar CrossRef Search ADS PubMed 16. Berenstein A , Kricheff II . Microembolization techniques of vascular occlusion: radiologic, pathologic, and clinical correlation . AJNR Am J Neuroradiol . 1981 ; 2 ( 3 ): 261 – 267 . Google Scholar PubMed 17. Berenstein A , Kricheff II . Catheter and material selection for transarterial embolization: technical considerations. II. Materials . Radiology . 1979 ; 132 ( 3 ): 631 – 639 . Google Scholar CrossRef Search ADS PubMed 18. Lasjaunias P . Vein of Galen malformations . Neurosurgery . 1989 ; 25 ( 4 ): 666 – 667 . Google Scholar CrossRef Search ADS PubMed 19. Lasjaunias P , Rodesch G , Pruvost P , Laroche FG , Landrieu P . Treatment of vein of Galen aneurysmal malformation . J Neurosurg . 1989 ; 70 ( 5 ): 746 – 750 . Google Scholar CrossRef Search ADS PubMed 20. Lasjaunias P , Rodesch G , Terbrugge K et al. Vein of Galen aneurysmal malformations. Report of 36 cases managed between 1982 and 1988 . Acta Neurochir . 1989 ; 99 ( 1-2 ): 26 – 37 . Google Scholar CrossRef Search ADS PubMed 21. Berenstein A , Niimi Y , Song J , Lasjaunias P . Vein of Galen aneurysmal malformation . In: Albright A , Pollack I , Adelson P , eds. Principles and Practice of Pediatric Neurosurgery , 2nd ed . New York : Thieme ; 2008 : 1014 – 1028 . Google Scholar CrossRef Search ADS 22. Hoang S , Choudhri O , Edwards M , Guzman R . Vein of Galen malformation . Neurosurg Focus . 2009 ; 27 ( 5 ): E8 . Google Scholar CrossRef Search ADS PubMed 23. Gailloud P , O’Riordan DP , Burger I et al. Diagnosis and management of vein of galen aneurysmal malformations . J Perinatol . 2005 ; 25 ( 8 ): 542 – 51 . Google Scholar CrossRef Search ADS PubMed 24. Paramasivam S , Niimi Y , Meila D , Berenstein A . Dural arteriovenous shunt development in patients with vein of galen malformation . Interv Neuroradiol . 2014 ; 20 ( 6 ): 781 – 790 . Google Scholar CrossRef Search ADS PubMed 25. Paramasivam S , Toma N , Niimi Y , Berenstein A . De novo development of dural arteriovenous fistula after endovascular embolization of pial arteriovenous fistula . J Neurointerv Surg . 2013 ; 5 ( 4 ): 321 – 326 . Google Scholar CrossRef Search ADS PubMed 26. Rodesch G , Lasjaunias P , Terbrugge K , Burrows P . Intracranial arteriovenous vascular lesions in children. Role of endovascular technics apropos of 44 cases . Neurochirurgie . 1988 ; 34 ( 5 ): 293 – 303 . Google Scholar PubMed Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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NeurosurgeryOxford University Press

Published: Jun 1, 2018

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