Endovascular management of vein of Galen ...

Childs Nerv Syst (2010) 26:1367–1379 DOI 10.1007/s00381-010-1257-0

SPECIAL ANNUAL ISSUE

Endovascular management of vein of Galen aneurysmal malformations. Influence of the normal venous drainage on the choice of a treatment strategy Monica Pearl & Juan Gomez & Lydia Gregg & Philippe Gailloud

Received: 16 July 2010 / Accepted: 26 July 2010 / Published online: 20 August 2010 # Springer-Verlag 2010

Abstract Introduction Vein of Galen arteriovenous malformations (VGAM) are rare intracranial vascular lesions mostly involving young children. Endovascular therapy is the current standard of care. Albeit interventional techniques have greatly reduced the once dismal vital and functional prognoses previously associated with these lesions, the treatment of VGAMs remains a complex therapeutic challenge. Discussions This article reviews the available endovascular options for VGAM therapy, emphasizing three points that we have identified as critical in our practice for the establishment of a treatment strategy: (1) the importance of the deep cerebral venous anatomy, in particular the existence of normal drainage through the Galenic system in spite of the VGAM; (2) the concept of treatment staging, for arterial as well as for venous interventions; and (3) the definition of a therapeutic goal that can be attained at a reasonable cost in terms of complication risks and functional outcome. Keywords Vein of Galen anomaly . Vascular malformation . Endovascular techniques . Venous anatomy . Internal cerebral veins A vein of Galen aneurysmal malformation (VGAM) is a rare vascular anomaly disproportionately represented in the pediatric population, where it is said to account for up to 30% of intracranial vascular malformations [10, 22]. A M. Pearl : J. Gomez : L. Gregg : P. Gailloud (*) Division of Interventional Neuroradiology, The Johns Hopkins Hospital, Baltimore, MD, USA e-mail: [email protected]

VGAM is defined by one or more arteriovenous shunts that drain into a dilated midline cerebral venous collector believed to correspond to the median prosencephalic vein of Markowski [28]. Although VGAMs are distinct from arteriovenous malformations (AVMs) or other arteriovenous fistulas (AVFs) that drain into enlarged but otherwise normal veins of Galen, these entities are sometimes considered together as they can present similar therapeutic challenges, in particular, when they become symptomatic early in life. This article will principally focus on the endovascular management of VGAMs, with emphasis placed on the drainage pattern of the deep venous system as an important factor in the choice of a treatment strategy.

Historical introduction Imprecise early observations of vascular malformations involving the vein of Galen reflect the difficulty of analyzing complex intracranial vascular anomalies without the help of modern angiographic techniques. Steinheil is often quoted as being the first author to describe an AVM involving the vein of Galen. In his 1895 publication [30] (cited by Pool and Potts [26]), he reports postmortem findings in a 49-year-old man with a frontal AVM draining into a dilated vein of Galen. Although this entity is not a true VGAM, it remains included in some modern VGAM classifications, in part as it can present similar therapeutic challenges in very young patients. Balance reports the first known attempt at VGAM therapy in 1905: his patient, an 11-month-old baby presenting with macrocephaly and increased intracranial pressure, was treated with bilateral carotid artery ligation (quoted by Pool and Potts [26]). The first detailed clinical description of a VGAM was published

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Fig. 1 VGAM classification (adapted from Yasargil [32]). a VGAM Type I: one or several direct arteriovenous shunts are connected to the aneurysmal venous collector of the VGAM. Compression of the cerebral aqueduct by the venous collector is illustrated. b VGAM Type II: an arterio-arterial, “nidus-like” network is interposed between the

arterial feeders and the venous collector. Note the presence of typical transmesencephalic thalamoperforators. c VGAM Type III: Type III is a combination of Types I and II. d VGAM Type IV: in this case, an arteriovenous malformation drains into an enlarged but otherwise normal vein of Galen

in 1937 by Jaeger, Forbes, and Dandy [15]. Later landmark publications include the report by Gold, Ransohoff, and Carter describing the various clinical pictures associated with VGAMs [10], and the work of Raybaud, Strother, and Hald dealing with the embryogenesis, morphology, and pathogenesis of the malformation [28].

resulting in high-volume blood shunting. The late presentation group (older children and adults) is associated with headaches, cognitive dysfunction, and, rarely, subarachnoid hemorrhage. VGAMs found in these patients typically consist of a complex, “nidus-like” arterio-arterial network responsible for milder arteriovenous shunting. Intermediate between these two clinical pictures is a delayed presentation group, made of infants and young children suffering from seizures, developmental delay, macrocephaly, and hydrocephalus, in whom the VGAM shows a combination of highflow shunts and arterio-arterial network. Of note, the presence of distended veins over the scalp and face is a classic, yet commonly overlooked diagnostic sign suggesting a high-flow intracranial vascular anomaly. There is no known maternal risk factor or genetic anomaly leading to the development of a VGAM. We have

Clinical presentation Not only are the three typical clinical presentations established by Gold et al. [10] in 1964 still valid nowadays, but they have been further substantiated by our current understanding of the VGAMs’ angioarchitecture. The early presentation group (neonates), characterized by cardiac and respiratory insufficiency, is associated with direct arteriovenous connections

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Fig. 2 Choroidal arteriovenous fistula (AVF) in a newborn baby presenting with cardiac and respiratory failure. a The choroidal AVF is located within the atrium of the right lateral ventricle. b The lesion is fed by multiple choroidal branches of the right posterior cerebral artery, and drains into an enlarged but otherwise normal vein of Galen (white arrow)

taken care of several patients with normal siblings, including two pairs of twins.

Angiographic classification A review of the various VGAM classifications that have been published so far is beyond the scope of this article. We find the categories established by Yasargil [32] particularly useful as they parallel the clinical pictures described by Gold and co-authors; they are used here in a slightly modified form. A VGAM Type I consisting of direct arteriovenous shunts established between the arterial feeders and the collecting vein is typically seen in the neonatal presentation with cardiorespiratory failure; the arterial feeders are typically choroidal branches of the pericallosal and posterior cerebral arteries (Fig. 1a). A VGAM Type II, with its transmesencephalic thalamoperforators feeding a complex arterio-arterial network interposed between the feeding arteries and the venous collector, is usually associated with a late presentation (Fig. 1b), while a VAGM Type III, made of a combination of Type I and Type II, is seen in the intermediate group of infants and children with delayed presentation (Fig. 1c). Of note, the occasional VGAMs incidentally discovered in asymptomatic adults have always been, in our experience, Type II lesions, a fact worth remembering when evaluating the risk versus benefit ratio of VGAM therapy. Finally, VGAM Type IV lesions correspond to arteriovenous malformations draining into an enlarged vein of Galen (Fig. 1d), i.e., the VGAD of Lasjaunias [16]. We like to also include in this group the high-flow choroidal AVFs that mimic the presentation of a VGAM and should be treated using similar techniques and strategies (Fig. 2). The Type III VGAMs are most common in our practice, as some arterio-arterial network is almost

always found in association with the high-flow lesions. This nidus-like component can be minimal at first and become more conspicuous after embolization of the direct arteriovenous shunts. Likewise, milder lesions diagnosed in infants and children frequently include a few direct arteriovenous connections within what could have at first appeared as a classic Type II VGAM. These observations suggest that the VGAM angioarchitecture is probably better described as an anatomopathological continuum rather than as distinct lesion types. However, in our experience, the combination of the Yasargil classification with the work of Gold and co-authors provides a useful tool for the practical management of patients with a VGAM, and a common vocabulary for the various members of the multidisciplinary treatment team.

Anatomical considerations In their superb contribution of 1986, Raybaud and colleagues [27] offered the first precise analysis of the morphological features of a VGAM. They also were the first authors to recognize the probable role of an embryonic precursor of the vein of Galen in the morphogenesis of the lesion, the median prosencephalic vein of Markowski [27, 28]. Of note, these authors observed and reported connections between the aneurysmal venous collector and normal deep venous channels in several of their specimens. VGAMs are a type of choroidal AVF believed to form between the 8th and 11th week of gestation. Their arterial feeders are therefore derived from the choroidal network, in particular the medial and lateral posterior choroidal arteries, but also the anterior choroidal artery (predominantly in neonates [28]), and the distal pericallosal artery (i.e., the superior posterior choroidal artery) [31]. Transmesencephalic branches arising from the basilar tip and the

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proximal posterior cerebral arteries are also common contributors to the arterial supply of VGAMs, particularly in Type II lesions. These branches, derived from the fetal mesencephalic arteries, are intimately linked to the devel-

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opment of the posterior lateral and medial choroidal arteries, derived from the fetal posterior choroidal and diencephalic arteries, respectively [25]. Far less common feeders, likely recruited secondarily, include the middle

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Fig. 3 VGAM diagnosed prenatally by maternal ultrasonography and magnetic resonance imaging (MRI). As the baby girl was stable at birth and during the immediate postpartum period, the treatment was postponed until the fourth month of life. a DSA, left vertebral artery injection, arterial phase, lateral view, showing a Yasargil Type III VGAM with several direct arteriovenous connections but also a small arterio-arterial component (not well appreciated in this image). Note the hypoplastic straight sinus (black arrow), a dominant falcine sinus (arrowhead), and a small occipital sinus (white arrow). b DSA, left common carotid injection, venous phase, lateral view, showing a second, smaller falcine sinus (white arrowhead) separately draining the inferior sagittal sinus (double white arrowheads). In addition, note the faint opacification of the venous collector (asterisk) due to antegrade drainage of an internal cerebral vein into the VGAM (long arrow). c MR venography, axial maximum intensity projection, showing multiple deep venous structures draining into the straight and falcine sinuses via the venous collector of the VGAM. These vessels include the left and right internal cerebral veins (long arrows), the right basal vein of Rosenthal (arrow), and a left atrial vein (arrowhead). d MRI, axial T2-weighted image obtained immediately before treatment at 4 months of age. Note the presence of mild internal and external hydrocephalus. e MRI, axial T2-weighted image obtained 6 weeks after transarterial embolization of the main arterial feeder with NBCA glue. Several small transmesencephalic fistulous connections resulting in a minimal amount of residual arteriovenous shunt have been left untreated. Note the reduction in the size of the venous collector, as well as in the resolution of both the internal and external hydrocephalus. A transvenous approach has been ruled out due to the presence of normal deep venous drainage into the Galenic system. The patient is neurologically and developmentally normal. f MRV, threedimensional rendering, sagittal projection obtained prior to therapy. The falcine sinus is the main drainage pathway for the VGAM. Note the hypoplastic straight sinus and a second falcine sinus separately draining the inferior sagittal sinus. One of the internal cerebral veins connected to the venous collector is visible (arrowhead). g MRV, three-dimensional rendering, sagittal projection obtained 6 weeks after embolization. The falcine sinus has collapsed and the venous collector of the VGAM has remodeled into a near normal vein of Galen/internal cerebral vein junction

cerebral artery, the superior cerebellar arteries, various meningeal branches (usually the posterior trunk of the middle meningeal artery), and the anterior thalamoperforating arteries [28]. Understanding the often-understated venous anatomy of a VGAM is critical for the choice of the most appropriate treatment strategy. The dilated midline venous collector, the landmark feature of a VGAM, appears to correspond to a persistent median prosencephalic vein of Markowski [28]. Most of this embryonic vessel is normally supposed to regress at the end of the choroidal phase, concomitantly with the development of the internal cerebral veins (ICVs), while its posterior end persists as the adult vein of Galen. In a VGAM, the whole channel remains patent, likely as a consequence of the establishment of abnormal arteriovenous connections with one or several choroidal arteries. The mechanism involved in the pathogenesis of the lesion remains obscure. Abnormal recanalization of an involuting/thrombosed venous channel, not unlike the supposed mode of formation of dural AVFs in adults, appears as an interesting hypothesis.

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VGAMs can drain through a normal straight sinus, and/ or through a falcine sinus, i.e., a persistent embryonic sinus that courses within the falx cerebri to join the posterior third of the superior sagittal sinus [28]. Variants include hypoplastic or absent straight sinuses, as well as multiple or sinuous falcine sinuses (Fig. 3a, b). The notion that the presence of a straight sinus precludes the existence of a VGAM is erroneous. From the confluence of the sinuses, the venous flow follows a normal path via the transverse and sigmoid sinuses to the internal jugular veins. Variants include prominent occipital and marginal sinuses, sometimes becoming the dominant drainage pathway towards the vertebral venous plexus, in particular when advanced highflow venopathy is present. Outflow impairment may lessen the hemodynamic consequences of the arteriovenous shunt and have a protective effect on the cardiac function [28]. However, it can at the same time worsen the intracranial venous hypertension and its deleterious effects on the brain parenchyma (Fig. 4a–c). The possibility of normal deep venous drainage through the Galenic system in patients with a VGAM has been a topic of debate. Although Raybaud et al. [28] reported the observation of a unilateral, nondilated ICV connected to the aneurysmal collector in several of their cases, the absence of normal drainage has been and continues to be a commonly described anatomic feature of VGAMs [1, 13, 19]. A classic assumption made throughout the literature has been that the deep venous system neither connects nor drains into the dilated median prosencephalic vein/vein of Galen [3, 17, 18]. This assumption is no longer tenable as such connections with the Galenic drainage have now been clearly documented in several published observations [9, 14, 21]. It is important to note that normal deep venous drainage through the Galenic system may not be apparent on angiograms or noninvasive imaging studies obtained prior to therapy, only to become conspicuous on follow-up studies [9]. Retrograde opacification of deep veins connected to the aneurysmal sac of the VGAM is only rarely observed during angiography, even in cases where such connections are documented by a noninvasive study obtained immediately prior to the angiogram, an indication that the direction of flow in these veins likely remains antegrade. When retrograde filling is seen, it is usually in patients with severe intracranial venous hypertension secondary to significant outflow impairment, a fact already mentioned by Yasargil [32] (Fig. 4a, b). This absence of visualization may be linked to technical factors related to the imaging equipment itself, or to hemodynamic phenomena, such as the preferential flow of contrast towards a high velocity shunt, or a siphon effect exerted upon the deep veins by the high-flow, low-resistance drainage into a dilated dural venous system in the absence of outflow impairment. It may also sometimes simply be due to the lack of attention usually

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Fig. 4 3-month-old boy referred to our institution for a VGAM Type III presenting with severe developmental delay, hydrocephalus, macrocephaly and seizures, without cardiac or respiratory repercussions. a DSA, right vertebral artery injection, arterial phase, lateral view, showing drainage through a prominent falcine sinus. Note the absence of a straight sinus, and the retrograde opacification of an enlarged internal cerebral vein (arrow). b DSA, right vertebral injection, venous phase, anteroposterior view, illustrating the anatomy of the venous drainage, in particular the presence of an occipital sinus (arrowhead) with bilateral marginal sinuses. Note the presence of bilateral stenoses at the sigmoid–jugular junction (arrows). c MRI, sagittal T1-weighted image, documenting severe hydrocephalus and cerebral atrophy, as

well as diffuse periventricular calcifications (hyperintensities surrounding the lateral ventricle). In this baby, venous outflow impairment likely had a protective effect from a hemodynamic standpoint (no cardiac or respiratory impact) while adding to the deleterious effect of venous hypertension upon the brain parenchyma. d MRI, sagittal T1weighted image obtained before treatment, showing compression of the cerebral aqueduct by the aneurysmal venous collector. Note the prominent internal cerebral vein (arrowhead). e MRI, sagittal T1weighted image after two transarterial embolization sessions. The size of the venous collector has decreased, and the aqueduct is now patent. The risk of permanent aqueduct compression following endovenous coiling is now reduced

paid to venous structures in general. In our experience, however, the observation of normal deep veins terminating in the venous collector of a VGAM prior to therapy is becoming more frequent, likely as an effect of constantly improving magnetic resonance imaging techniques (Fig. 3c). The documentation of normal deep venous drainage into the Galenic system is a critical element of the treatment planning (Fig. 3d–g). One of the authors of this article has been shown many cases by colleagues who were distressed to see a VGAM patient successfully treated via a transvenous approach die or become significantly impaired, a few minutes to a few days after the procedure, from massive basal ganglia and/or intraventricular hemorrhage. These adverse events are generally considered to be consistent with the natural

history of the lesion or to represent a technical complication of the endovenous procedure (vessel perforation, aneurysmal sac rupture) [23]. In our opinion, they rather represent, for the most part, a hemodynamic complication related to the impairment of the normal deep venous drainage, namely deep venous infarction. The goal of endovenous embolization is to pack the venous collector of the VGAM with embolic material (coils or liquid agents) in order to shut down the arteriovenous connections draining into it. However, the procedure will at the same time impair flow in the deep veins potentially ending into the venous collector. The combination of deep venous ischemia with the local surge in arterial blood pressure taking place after rapid and complete obliteration of the arteriovenous shunts (akin to the normal perfusion pressure breakthrough phenomenon described by Spetzler

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Fig. 5 Baby girl presenting at birth with cardiac and respiratory failure, successfully managed by three sessions of transarterial embolization during the first week of life. After an initially favorable follow-up, she was readmitted emergently at 1 month of age for severe, life-threatening pulmonary hypertension. Transvenous embolization was elected. The pulmonary pressure remained elevated throughout the procedure, decreasing only as the coiling of the venous collector became close to complete. The post-treatment period was

favorable, with a neurologically intact baby and resolution of the pulmonary hypertension. She became comatose 72 h after the embolization; a head CT was obtained immediately. a Head CT showing diffuse basal ganglia (arrow) and intraventricular hemorrhage (arrowhead). b Compare the pattern of hemorrhage illustrated in a with this photography depicting the typical postmortem appearance of infarction following deep cerebral venous thrombosis (from [11] with permission)

and coauthors [29]) can certainly explain the almost constant hemorrhagic transformation occurring in these deep venous infarcts (Fig. 5a, b).

aneurysmal venous collector through a transarterial approach, while an arterial feeder that is difficult or impossible to selectively catheterize directly can occasionally be reached via a retrograde transvenous route. We believe that, for VGAMs as for other complex intracranial vascular malformations, staging the treatment in multiple embolization sessions is a key factor in achieving a successful outcome. Staging offers a more controlled devascularization process that helps prevent adverse events such as a normal perfusion pressure breakthrough phenomenon or a massive venous thrombosis [8]. Treatment staging is a relatively wellaccepted concept for transarterial embolization. We suggest that staging is equally important for endovenous procedures. Unfortunately, critically ill patients, e.g., newborns in cardiorespiratory failure or children developing malignant pulmonary hypertension, do not always allow for the luxury of a staged approach (as seen in see Fig. 5). Occasionally, a lesion vascularized by a single or largely dominant arterial feeder will ipso facto prevent a staged transarterial approach (Fig. 6). The timing of the first treatment session in neonates essentially depends upon the degree of cardiac and respiratory insufficiency caused by the VGAM. Early intervention offers the advantage of using an umbilical route. However, in newborn babies presenting without cardiorespiratory impairment and without significant hydrocephalus, e.g., in cases detected by maternal sonography and following normal developmental patterns, we prefer to delay the first

Endovascular techniques A comprehensive, multidisciplinary approach is essential to the optimal management of patients with VGAMs. Improvements in pediatric and neonatal intensive care along with advances in endovascular techniques and materials have significantly improved the historically dismal vital and functional prognoses associated with VGAMs [8, 20]. Treatment now relies almost exclusively on endovascular methods, with surgery reserved for the evacuation of intracranial hematomas and the management of hydrocephalus [12]. Surgical treatment of hydrocephalus, accomplished by ventriculoperitoneal (VP) shunting or by endoscopic third ventriculostomy [7], should only be used as a last resort measure, after failure of the endovascular therapy to correct the ventricular enlargement. Endovascular therapy can either target the arterial side or the venous side of the VGAM by blocking the arteries feeding the arteriovenous shunts or by obliterating the aneurysmal venous collector draining the lesion. In either case, access to the treatment site can be obtained via a transvenous or a transarterial route. For example, large arteriovenous connections commonly offer access to the

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Fig. 6 Newborn baby presenting with cardiorespiratory failure from a VGAM Type I (courtesy of Dr. Dawson). A dominant feeding artery was successfully treated by transarterial embolization, with excellent initial follow-up. a Head CT obtained immediately after embolization showing no change in the size or configuration of the venous collector. b Head CT obtained 28 days after treatment. The venous collector has decreased in size and shows partial thrombosis. A ventricular catheter has been placed. c Head CT obtained 30 days after treatment. The thrombus has slightly progressed and there is evidence of fresh intraventricular hemorrhage. d Head CT obtained 35 days after treatment. Progression of the thrombus led to complete obliteration of the venous collector

embolization until the fourth month of life, at which time the baby has gained in overall strength, and the diameter of the femoral arteries allows for the repeated accesses inherent to staged therapy. It is important to keep in mind the concept of therapeutic window proposed by Lasjaunias [19]: an excessive delay before treatment may lead to permanent impairment of the cerebrospinal fluid hydrodynamics, after which successful correction of the arteriovenous shunts may not result in hydrocephalus regression. By staging our first embolization at 4 months, we are able to perform two or three sessions before the 6-month barrier, using either our routine 6- to 8-week interval between procedures, or a shortened 4-week interval for particularly complex lesions. A detailed description of the techniques and materials involved in the endovascular management of intracranial vascular malformations lies beyond the scope of this article. It should be noted, however, that a large part of the devices and treatment agents routinely utilized for

this purpose are used on an off-label basis. As the field of pediatric neurovascular disorders, with its small number of potential patients, lacks a strong financial appeal to medical companies, physicians have to rely on devices and agents developed for the adult population. Technical parameters that are specific to or particularly sensitive for children (toxicity, radiation exposure, etc.) are usually neither evaluated nor addressed. Some device manufacturers go as far as preventing the use of approved devices in the pediatric population (microcatheters commonly used in adult patients, for example) by stating, for no apparent reason other than maybe liability avoidance, that the use of their products is “contraindicated in infant and children”. The following account should be viewed as an example of practice, reflecting, in terms of technique and device selection, the experience and personal preferences of the authors. The management principles proposed below are, on the other

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Fig. 7 Second transarterial embolization session of a newborn baby boy with VGAM Type I presenting with cardiac and respiratory failure. a DSA, right internal carotid artery injection, lateral view. Note the typical branches from the pericallosal and posterior cerebral arteries feeding several high-flow direct arteriovenous shunts. b DSA, superselective injection of a posterior-superior choroidal branch (pericallosal artery termination), lateral projection. The proximal portion of this feeding branch has an irregular appearance initially believed to represent some tortuosity, but corresponding in fact to a pseudoaneurysmal expansion of the vessel. It was decided to include

that dysplastic segment in the embolization target. The microcoil partially projecting over the feeder was placed during a previous session in a separate branch. In spite of a wide caliber and fast flow, the length of the targeted segment is in this case sufficient for adequate glue deposition, and the adjunct use of a coil is not necessary. c DSA, superselective injection of the posterior-superior choroidal branch with NBCA (near-pure glue concentration). The radio-opaque glue is casting the targeted segment, including the pseudoaneurysmal component, while the white tract corresponds to the subtraction artifact left by the microcatheter that has already been withdrawn

hand, independent from the specific tools chosen for the performance of the described procedures.

umbilical artery in neonates [6]. In our practice, staged procedures have been performed through an umbilical access maintained for up to 1 week. For conventional femoral access, we routinely use 4-French systems for diagnostic as well as therapeutic purposes in all pediatric age categories. We prefer placing an arterial sheath, in spite of its slightly larger diameter, to direct access of the femoral artery with a diagnostic or guiding catheter. This approach,

Transarterial embolization Transarterial embolization is well established and, in our institution, is the favored initial therapeutic approach whenever possible. Arterial access is obtained through the

Fig. 8 4-month-old baby girl with VGAM Type III (same child as Fig. 3). Transarterial embolization of a direct arteriovenous shunt fed by a posterior-lateral choroidal artery. a DSA, superselective injection of a posterior-lateral choroidal branch, lateral projection, showing a high-flow single-hole shunt. Note the large caliber of the feeder and the short segment of vessel available for glue deposition. In such an anatomic configuration, we find it beneficial to deliver a microcoil prior to glue injection. b DSA, superselective injection of a posteriorlateral choroidal branch, lateral projection, after delivery of a single

microcoil. Note that flow velocity is barely impaired by the device. The benefit of deploying a coil prior to NBCA embolization lies more in offering a scaffold for the glue to attach to rather than inducing a significant change in flow pattern. c DSA, superselective injection of a posterior-lateral choroidal branch with NBCA (near-pure glue concentration). The opaque glue lies within the targeted arterial segment; the microcatheter has already been withdrawn (white subtraction artifact)

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which reduces the risk of potential injury to the femoral artery by avoiding torsion and sliding motion at the puncture site, has proved effective and safe in our experience (no groin or leg complication recorded in 241 consecutive pediatric cerebral angiograms) [2]. Superselective catheterization of the VGAM arterial feeders can

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be performed using a selection of microcatheters and microwires made on an individualized basis, largely based on operator’s preference. Transarterial embolization is ideally performed with a liquid embolic agent, with or without the adjunct use of detachable microcoils (Figs. 7a–c and 8a–c). Relying on microcoils alone is not

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Baby boy with a Type I VGAM initially treated at an outside institution by coiling of one feeding artery, referred to our center at age three for further therapy (a). A first transarterial session was performed, during which several arterial feeders were embolized with NBCA glue. During a second transarterial session, 2 months later, access to the venous collector was gained through one of the remaining arteriovenous shunts. Several coils were detached within the venous aneurysm. The microcatheter was then withdrawn and the arterial side of the feeder embolized with NBCA glue (b). The remainder of the venous collector was obliterated with microcoils during a third embolization session 6 months later (c). The clinical follow-up was uneventful, with normal neurological and cognitive development 5 years after treatment. MR imaging studies obtained 6 months and 2 years after the procedure document the presence of normal deep venous structures draining through the Galenic system (d–g). a DSA, right vertebral artery injection, AP projection prior to treatment. Note the presence of moderate bilateral venous outflow impairment, which likely had some protective effect on the cardiac function without major repercussion on the cerebral parenchyma and cerebrospinal fluid hydrodynamics. b DSA, left vertebral artery injection, AP projection after partial coiling of the venous collector and NBCA embolization of one additional arterial feeder. Residual flow within the venous aneurysm is intentionally left as part of a staged endovenous obliteration strategy. Note the presence within a choroidal branch of the right posterior cerebral artery of the microcoils delivered at an outside institution. c DSA, left vertebral artery injection, AP projection after near complete obliteration of the venous collector. A minimal amount of contrast agent can be seen stagnating within the coil pack, without angiographically detectable outflow to the falcine sinus. No angiographic visualization of the normal deep venous system at this stage. d MR imaging, axial T2-weighted image obtained 6 months after treatment. The venous collector content shows heterogeneous signal consistent with a combination of coil material and thrombus. e MR angiography, craniocaudal maximum intensity projection, showing no detectable residual arteriovenous shunts. f MR venography, craniocaudal maximum intensity projection, illustrating the course of both internal cerebral veins (arrowheads) coursing toward the medial aspect of the coiled venous collector (short arrow) and draining into the straight sinus (long arrow). g MR venography, sagittal maximum intensity projection, showing drainage of both internal cerebral veins (arrowheads) though the coiled venous collector (short arrow) into the straight sinus (long arrow)

recommended, as these devices do not generally offer sufficient penetration of the feeding branches, and may therefore only offer a temporary effect. In addition, the risk of rupture or perforation while delivering a microcoil in a fragile arterial feeder is not negligible, a situation in which immediate injection of a fast-acting liquid agent may be essential in avoiding a devastating complication. There are two liquid embolic agents currently available in the United States: N-butyl-cyanoacrylate (NBCA) (Trufill, Codman Neurovascular, NJ) and ethylene vinyl alcohol copolymer (Onyx, MicroTherapeutics, CA). The respective advantages and disadvantages of these two products are beyond the scope of our article. The treatment of a VGAM with either of these agents represents an off-label indication. Our liquid embolic agent of choice is NBCA mixed with ethiodized oil. The NBCA-to-ethiodized oil ratio modulates

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the setting characteristics of the mixture, which can be tailored to the specific hemodynamic and angioarchitectural features of the VGAM, allowing precise targeting of the arteriovenous shunt. In our practice, transarterial embolization aims at the arterial feeders only; obliteration of the aneurysmal venous collector with a liquid embolic agent injected from the arterial side is not performed for reasons that will be discussed below. Transvenous embolization Transvenous VGAM therapy is, from a technical standpoint, significantly less challenging than transarterial embolization. The relative lack of control offered by endovenous coiling and the potential repercussions associated with deep venous drainage impairment must, however, be carefully weighed against technical ease when choosing a therapeutic strategy. In our practice, the endovenous approach comes into play when the transarterial route has been exhausted, i.e., when all the arterial feeders that could safely be targeted have been embolized. One of the advantages of embolizing the arterial feeders of a VGAM rather than its venous collector is to avoid the persistence of the mass effect it exerts upon the surrounding cerebral tissue. For example, packing with microcoils a venous collector that causes noncommunicating hydrocephalus by compression of the cerebral aqueduct is unlikely to decrease the ventricular enlargement. In this situation, even when an endovenous treatment is planned, preparation of the lesion with arterial embolization can prove beneficial (Fig. 4d, e). Venous access is gained by puncture of the femoral vein. A jugular vein access or even a direct puncture of the torcular may be considered in exceptional situations [4, 5, 24]. As noted earlier, a transvenous approach can occasionally be used for arterial embolization via retrograde catheterization of a direct arteriovenous shunt [5]. Conversely, venous access is at times gained during transarterial embolization by passage of the microcatheter across a direct arteriovenous shunt into the aneurysmal collector. This (sometimes unintentional) access to the venous side can be used to deliver a few microcoils and form an initial coil frame within the VGAM collector (in our practice, this is done only when the ongoing procedure is expected to be the last transarterial session of a staged treatment plan that includes a subsequent endovenous approach). Our preference goes, in that instance, to long detachable coils with a larger coil diameter (GDC 18, Boston Scientific, Natick, MA). The microcatheter is then withdrawn into the arterial feeder, and a glue injection performed as initially planned. We believe treatment staging to be as important for endovenous procedures as it is for arterial embolization. In either case, staging helps preventing the abrupt change in locoregional hemodynamic conditions that can lead to a

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normal perfusion pressure breakthrough phenomenon by offering a more progressive readjustment of the arterial flow previously aimed toward the high-volume shunts. Similarly, we propose that staging endovenous procedures may help decrease the incidence of deep venous infarcts by allowing some redistribution of the normal venous territories that drain through the Galenic venous system in spite of the VGAM. Finally, we believe that observing minor residual flow within a venous collector that is nearly completely packed with coils should not be perceived as a negative occurrence. Magnetic resonance imaging and venography obtained either as a follow-up study or immediately before the next planned embolization session (as it is the case in our practice) can help decide whether further therapy is necessary or, on the contrary, should be avoided, considering the evolution of the risk versus benefit ratio following each therapeutic step (Fig. 9).

Conclusions The successful treatment of VGAMs remains a complex therapeutic challenge. This article offers a few strategic considerations for the treatment of these lesions, which can be summarized along the following lines: Importance of the normal venous anatomy While this fact has long been ignored or considered irrelevant, it is now clear that connections can exist between deep cerebral veins and the venous collector of a VGAM. The exact role of these connections remains debatable. We propose that the basal ganglia and intraventricular hemorrhages observed after endovenous VGAM treatment are, for the most part, related to impairment of the deep venous drainage. The frequent, if not constant hemorrhagic transformation of the resulting deep venous infarcts is likely related to the disturbance simultaneously imposed on the arterial side of the lesion, similar to a normal perfusion pressure breakthrough phenomenon, which brings a sudden surge in blood pressure in cerebral territories already fragilized by ischemia. Role of treatment staging for arterial and venous procedures The importance of treatment staging has been generally recognized for arterial embolization. When allowed by the patient’s clinical condition, staging offers a more controlled and gradual devascularization process that is believed to reduce the risk of adverse events such as diffuse venous thrombosis or normal perfusion pressure breakthrough phenomenon. We propose that staging endovenous procedures is equally important in terms of complication avoidance.

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Besides a less abrupt change in the arterial circulation, staging endovenous embolization may also offer time for the venous system to adapt to new drainage patterns, in particular when one or several deep venous channels are connected with the Galenic system. We have illustrated the important role played by magnetic resonance imaging and venography obtained immediately before endovascular therapy as a means to evaluate the risk to benefit ratio of each planned embolization session. Definition of a therapeutic goal From an endovascular perspective, it may be said that any cerebral vascular malformation can be embolized completely, using almost any available therapeutic agent. The question then lies in the price associated with the total eradication of a lesion in terms of mortality, morbidity, and quality of life. Although a discussion of this complex point is beyond the scope of our article, we believe that a physiological cure of a VGAM that leaves part of the vascular malformation untreated but leads to favorable neurological and developmental outcomes may be preferable to an anatomic cure, more definitive but associated with high complication rates and potentially dismal outcomes. The importance of a close and truthful communication with the parents (and the patient when possible) is essential in guiding these choices, taking into account that individual presentations, ranging from newborn babies in cardiorespiratory distress to asymptomatic young adults, come with specific levels of urgency and risk acceptance.

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