29 Endovascular Management of Brainstem and Thalamic Arteriovenous Malformations

10.1055/b-0039-173920

29 Endovascular Management of Brainstem and Thalamic Arteriovenous Malformations

Fadi Al-Saiegh and Pascal M. Jabbour

Abstract

Endovascular management of brainstem and thalamic arteriovenous malformations (AVMs) requires the use of cerebral angiography to determine the nature and extent of these abnormal connections between the arterial and venous vasculature, which have no intervening capillary bed allowing for high-flow shunting of blood. Cerebral angiography is indispensable for identifying the diameter and number of arterial feeders, the involvement of brainstem and thalamic perforators, the venous drainage pattern, and the architecture of the nidus. AVMs occur with an incidence of 1 in 100,000. However, deep-seated AVMs of the thalamus and brainstem constitute a small subgroup of 2 to 6% of all AVMs and carry an annual risk of rupture of 9.8 to15%. The goal of treatment is complete obliteration of the AVM. Endovascular embolization can be used as a curative modality or as an adjunct to microsurgery or radiosurgery. Presurgical embolization is particularly useful when arterial supply is inaccessible or bilateral, as it can obviate the need for staged operations. Embolization can also be used for nidal volume reduction, thus lowering the margin dose to the radiosensitive thalamus and brainstem, and it is particularly useful in patients with acutely ruptured AVMs. Curative embolization can be achieved in certain patients with a small nidus and limited venous and arterial channels. Aside from conventional single-artery liquid agent embolization, some AVMs can be embolized using double-arterial or transvenous routes and using solid agents. The main complications related to embolization result from ischemic or hemorrhagic events from emboli or vascular injury, respectively, with an overall morbidity rate of zero to16.7%. Because of their complexity, brainstem and thalamic AVMs require expertise in endovascular techniques to maximize the benefits from this treatment modality.

Pathophysiology, Epidemiology, and Natural History

Arteriovenous malformations (AVMs) of the brain are characterized by a network of dysplastic vessels with no intervening capillary bed. The lack of normal capillaries results in a high-flow low-resistance connection between arterial feeders and venous channels that allows the transmission of arterial pressure into the thin-walled draining veins, which leads to venous dilatation and hypertension. Central to this connection is a network of abnormal vessels between the distal feeding arteries and the proximal draining veins that is termed the nidus. The high-flow arteriovenous shunting across the nidus gives AVMs their angiographic hallmark, namely early opacification of the venous channel and a shortened transit time. The nidus may contain gliotic tissue and is the site of various pathologic processes resulting in edema, tissue inflammation, and hemodynamic derangements that collectively contribute to its high propensity to rupture. At the same time, the nidus is the primary target site for endovascular embolization.

Cerebral AVMs occur with an incidence of 1 in 100,000 per year, with equal sex distribution, and are most commonly diagnosed by the fourth decade of life. ¹ ^, ² ^, ³ ^, ⁴ Their natural history is influenced by a variety of factors. The overall annual cumulative risk of rupture is 2 to 4%, ⁴ ^, ⁵ ^, ⁶ ^, ⁷ which increases to 6% in the first year after the initial hemorrhage. ⁸ Hypertension, high-feeding artery pressure, ⁹ intranidal aneurysms, ¹⁰ deep venous drainage, and a small nidus size (< 3 cm) ⁹ have all been recognized to increase the risk of hemorrhage. Another important risk factor is the location of the AVM. Deep-seated cerebral AVMs, such as those located in the brainstem and thalamus, have been associated with a higher risk of hemorrhage than other cerebral AVMs. Brainstem and thalamic AVMs constitute 2 to 6% of all intracranial AVMs. ¹ ^, ³ ^, ¹¹ ^, ¹² ^, ¹³ Substantial evidence suggests that brain-stem and thalamic AVMs have a more aggressive natural history than their lobar convexity counterparts and that patients tend to present at a younger age (mean 22.7 vs. 29.0 years, respectively). ¹⁴ The annual rupture rate for brainstem and thalamic AVMs is reported as 9.8 to 15%, ¹³ ^, ¹⁵ with a similar rerupture rate of 17.8% ⁷ that increases to 34% with exclusive deep venous drainage. ¹⁶ They also carry a higher risk of hemorrhage-related mortality of up to 62.5%. ¹⁷ These AVMs pose an enormous challenge even with current treatment modalities, and because of their rarity and complexity, no single management strategy can be formulated universally.

Anatomical Classification and Vascular Supply of Brainstem AVMs

Brainstem AVMs occupy one of the most delicate areas of the brain and are in close vicinity to cranial nerves (CNs) and their nuclei as well as important vascular structures and fiber tracts. Because their precise location and vascular supply have implications for treatment and outcome, this type of AVM has been classified into several subtypes in surgical case series. ¹³ ^, ¹⁸ This differentiation is similarly valuable in endovascular management because it aids better understanding of the vascular anatomy. Accordingly, brainstem AVMs can be seated on the anterior or posterior midbrain surface, the anterior or lateral pons, or the anterior or lateral medulla oblongata. Anterior mesencephalic AVMs are adjacent to the cerebral peduncles and the oculomotor nerve (CN III) and are supplied by the P1 segment of the posterior cerebral artery (PCA) and the anterior choroidal artery and are mostly drained by the median anterior mesencephalic vein. Posterior mesencephalic AVMs are located on the tectal or pineal surface in proximity to the trochlear nerve (CN IV) and are usually fed by bilateral perforators of the PCA, superior cerebellar artery (SCA), or posterior inferior cerebellar artery (PICA). This group is drained by tributaries of the vein of Galen. Further caudally, arterial feeders of pontine AVMs are usually derived from branches of the anterior inferior cerebellar artery, PICA, and SCA. Anteriorly located pontine AVMs may receive additional feeders from the basilar artery; however, this is less likely for laterally located AVMs that extend into the cerebellopontine angle. Both pontine AVM variants may flank the trigeminal nerve (CN V) root and are drained by the superior petrosal vein and sinus. At the level of the hypoglossal nerve (CN XI) rootlets, anterior medullary AVMs receive feeders from the V4 segment of the vertebral arteries and lateral medullary AVMs may be supplied by additional branches from the PICA. Both drain into the anterior mesencephalic vein, but lateral medullary AVMs can also drain into the lateral medullary vein. The nidus of mesencephalic, pontine, and medullary AVMs can lie within the parenchyma or extrapially in the subarachnoid space.

Anatomy and Vascular Supply of Thalamic AVMs

Thalamic AVMs are located medial to the posterior limb of the internal capsule. Within the thalamus, they can be located superiorly where they border the floor of the lateral ventricle or medially adjacent to the lateral wall of the third ventricle. In a series of 22 thalamocaudate AVMs, arterial feeders were derived from a combination of posterior choroidal and posterior pericallosal arteries in 13 cases, followed by the distal anterior pericallosal artery in 9 cases, and less commonly by the anterior choroidal artery in 4 cases. ¹⁹ Other series have documented a primary supply of the nidus by thalamoperforators of the proximal PCA and posterior communicating artery as well as by the medial and lateral posterior choroidal artery, the anterior choroidal artery, and, less commonly, the lenticulostriate arteries. ¹² ^, ²⁰ The venous drainage of these deep-seated AVMs is accomplished by the thalamostriate and internal cerebral veins medially or the basal vein of Rosenthal inferiorly. ¹² ^, ²⁰

Clinical Presentation

Patients who harbor a brain AVM may manifest a variety of clinical symptoms. Across all intracranial locations, the most common initial presentation of AVMs is subarachnoid, intraparenchymal, or intraventricular hemorrhage, which occurs in about 50% of patients. ³ ^, ²¹ ^, ²² ^, ²³ The second most common presenting symptom is seizures, which occur in approximately 20 to 30% of patients, ² ^, ³ ^, ²³ followed by chronic headache, which occurs in about 5 to 15%. ³ ^, ²³ In the subgroup of deep-seated vascular malformations, such as those involving the brainstem or thalamus, initial hemorrhagic presentation is substantially higher with rates in the range of 70 to 90%. ³ ^, ¹¹ ^, ¹³ ^, ¹⁵ ^, ²⁴ ^, ²⁵ ^, ²⁶ Rupture of AVMs in these eloquent locations produces severe neurologic deficits, including hemiparesis, hemiplegia, and hemianesthesia, in as many as 85% of patients. ¹⁵ ^, ²⁰ This figure stands in contrast to the 84% (97/115) of patients with no or mild neurologic deficits (Rankin Scale score of 0 or 1) in a study of overall AVM rupture-related morbidity. ²⁷ Brainstem AVMs can also cause CN palsies. Lesions in the cerebellopontine angle often cause dysfunction in the trigeminal, abducens, facial, and vestibulocochlear nerves (CNs V–VIII) dysfunction and pontine AVMs can affect the trigeminal, abducens, facial, vestibulocochlear, glossopharyngeal, and vagus nerves (CNs V–X), causing facial pain, facial weakness, speech difficulty, and ataxia. ¹¹ ^, ²⁸

It is not entirely clear why patients with thalamic and brain-stem AVMs more frequently present with a hemorrhage than patients with cerebral convexity AVMs. However, in a cohort of 3,299 patients, Tong et al ³ found that this AVM subgroup is also less likely to present with seizures than those with cerebral convexity AVMs. Therefore, it is conceivable that the decreased propensity to cause seizures keeps these AVMs clinically silent and is accountable for a relative increase in hemorrhagic presentation. ²⁹ Another explanation for the increased frequency of hemorrhages may be the higher association of aneurysms in some of these deep AVMs. ¹⁴

Preoperative Evaluation

The initial radiographic evaluation of brainstem and thalamic AVMs commonly includes computed tomography in the acute setting, which is followed by magnetic resonance imaging and digital subtraction angiography. Magnetic resonance imaging allows determination of the precise location and size of the AVM, whereas digital subtraction angiography provides detailed information on the AVM characteristics and is indispensable in planning therapy. Because thalamic and brainstem AVMs are uniformly located in eloquent areas and have deep venous drainage, they are classified as a Spetzler-Martin grade III or greater by default ³⁰ ; however, this grading system only distinguishes among the sizes of these AVMs. Therefore, the preoperative evaluation of brainstem and thalamic AVMs is dependent on thorough angiographic characterization by selective injection of the major cerebral vessels and the AVM itself, followed by super-selective injection of the nidus using microcatheters. The goal of the selective injection is to identify the caliber and number of arterial feeders, possible flow-related aneurysms, the hemodynamics of the AVM, the size and compactness of the nidus, and the venous drainage pattern. The superselective injection provides detailed information about the nidus angioarchitecture, presence of intranidal aneurysms or outlet obstructions, venous ectasias or varices, nidal compartments, ³⁰ and—very importantly in brainstem and thalamic AVMs—the involvement of perforators in the supply of the nidus.

Diagnostic angiography is also used to assess the technical feasibility of endovascular management. It serves as a practical test of the accessibility of the arterial feeders and the nidus. Super-selective microcatheterization is required for safe and successful embolization and depends not only on the caliber of but also on the tortuosity of the feeding pedicles. Accessibility of the nidus and analysis of the angiographic features help the endovascular surgeon determine the role of embolization in the treatment of an individual AVM.

Endovascular Management

The goal of any definitive treatment strategy for brainstem and thalamic AVMs is complete obliteration of the nidus to eliminate the risk of hemorrhage-related morbidity and mortality. Endovascular embolization provides a minimally invasive approach in the management of these AVMs and can be used with adjunctive, palliative, or curative intent.

Endovascular Embolization as an Adjunct to Microsurgery

Endovascular embolization has traditionally been used adjunctively to enhance the safety and efficacy of microsurgical AVM resection. Its goal is to devascularize the AVM by occluding deep surgically inaccessible feeders, decreasing the size of the nidus, and occluding intranidal aneurysms. It can also facilitate AVM extirpation by serving as a surgical road map and affording a better defined dissection plane. In addition, embolization can reduce operative time and blood loss from fragile dysplastic vessels, which is especially valuable in thalamic AVMs, where bleeding at the periphery of the nidus can require more extensive dissection in eloquent tissues in order to achieve hemostasis, thus increasing surgical morbidity. ³¹ In brainstem AVMs, presurgical embolization is particularly beneficial in lesions with bilateral arterial feeders, which are often seen in AVMs located in the dorsal midbrain; this procedure can be used to occlude feeders contralateral to the surgical exposure to avoid a multistage operation. ¹³ It is also effective in cerebellopontine angle AVMs, which often have a triple vascular supply from the anterior inferior cerebellar artery, PICA, and SCA. ¹³ In such cases, preparatory embolization may obviate the need for an extended retrosigmoid exposure to control all arterial feeders and allow resection. Moreover, presurgical embolization has the potential of converting high-grade Spetzler-Martin AVMs to lower-grade lesions, possibly making them amenable to surgery. In their case series of multimodality treatment of deep-seated AVMs, Lawton et al ³² reported three lesions that were initially considered inoperable but were resected in a single-stage after endovascular embolization. The authors recommended preoperative embolization followed by resection for surgically accessible AVMs.

Endovascular Embolization as an Adjunct to Stereotactic Radiosurgery

Endovascular embolization can be combined with stereotactic radiosurgery (SRS) to treat brainstem and thalamic AVMs. Radiosurgery has been shown to be effective in the management of small to moderately sized AVMs. However, large AVMs of the brainstem and thalamus pose a challenge for SRS because of lower obliteration rates compared to AVMs located elsewhere. ¹ ^, ¹⁴ ^, ³³ A higher obliteration rate of these AVMs can be achieved with a higher prescription dose targeted at the AVM nidus. ³⁴ ^, ³⁵ However, the brainstem and thalamus are particularly radiosensitive and do not tolerate large amounts of radiation-induced changes without permanent neurologic deficits. ³⁶ Kiran et al ¹⁴ retrospectively analyzed the outcome of 53 AVMs in the thalamus, basal ganglia, and brainstem and 255 AVMs at other locations. They observed a significantly higher incidence in deep-seated AVMs compared to others of radiation-induced edema (15% vs. 5%, respectively) and lower obliteration rates (3-year actuarial obliteration rates, 68% vs. 76%, respectively). Furthermore, the sole use of SRS in ruptured thalamic or brainstem AVMs is suboptimal in light of the continued high risk of a recurrent, potentially fatal, hemorrhage during the latency period of 2 to 5 years. ¹ ^, ³⁵ ^, ³⁷ In such cases, preradiosurgical embolization can serve to reduce the effective volume of the nidus so that the residual can be targeted with a lower margin dose and thus incur potentially less adverse radiation effects. ³⁸ ^, ³⁹ Unfortunately, data are equivocal on whether nidal volume reduction by embolization translates into higher obliteration rates of the AVM after SRS. ⁴⁰ A meta-analysis that included 1,988 patients found that embolization before SRS decreased the AVM obliteration rate from 59% in the group without prior embolization to 41% after embolization, without increasing the rate of hemorrhage or permanent neurologic deficits. ⁴¹ Some authors argue that the embolization material may scatter or absorb ionizing radiation beams and thus decrease the obliteration rate. ¹ The risks should be carefully weighed against the benefits in each case. Yet, endovascular embolization should be strongly considered in freshly ruptured AVMs with high blood flow to the nidus, intranidal aneurysms, and venous varices because embolization can address these dangerous features to reduce the risk of rerupture with no latency period ( Fig. 29.1 ). ⁴² Lastly, endovascular embolization is also an option for AVMs that are refractory to or only show partial obliteration after SRS. ⁴³