Endovascular management of vein of Galen aneurysmal malformations. Influence of the normal venous drainage on the choice of a treatment strategy
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- Pearl, M., Gomez, J., Gregg, L. et al. Childs Nerv Syst (2010) 26: 1367. doi:10.1007/s00381-010-1257-0
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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.
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.
KeywordsVein of Galen anomalyVascular malformationEndovascular techniquesVenous anatomyInternal 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 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 . 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.
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  (cited by Pool and Potts ), 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 ). The first detailed clinical description of a VGAM was published in 1937 by Jaeger, Forbes, and Dandy . Later landmark publications include the report by Gold, Ransohoff, and Carter describing the various clinical pictures associated with VGAMs , and the work of Raybaud, Strother, and Hald dealing with the embryogenesis, morphology, and pathogenesis of the malformation .
Not only are the three typical clinical presentations established by Gold et al.  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 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 high-flow 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 taken care of several patients with normal siblings, including two pairs of twins.
In their superb contribution of 1986, Raybaud and colleagues  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 ), and the distal pericallosal artery (i.e., the superior posterior choroidal artery) . Transmesencephalic branches arising from the basilar tip and the 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 development of the posterior lateral and medial choroidal arteries, derived from the fetal posterior choroidal and diencephalic arteries, respectively . Far less common feeders, likely recruited secondarily, include the middle cerebral artery, the superior cerebellar arteries, various meningeal branches (usually the posterior trunk of the middle meningeal artery), and the anterior thalamoperforating arteries .
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 . 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.
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.  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 . 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  (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 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).
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 . Surgical treatment of hydrocephalus, accomplished by ventriculoperitoneal (VP) shunting or by endoscopic third ventriculostomy , should only be used as a last resort measure, after failure of the endovascular therapy to correct the ventricular enlargement.
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 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 : 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 hand, independent from the specific tools chosen for the performance of the described procedures.
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 . 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.
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. 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.