15 Deep Arteriovenous Malformations

The insula is a triangular-shaped structure covering the lateral surface of the central core, with the triangle’s base under the frontal operculum and its apex directed anteriorly and inferiorly toward the limen insulae (Fig. 15.1a). The insula is divided into anterior and posterior parts by the central sulcus of the insula, which runs parallel and deep to the central sulcus of the convexity. The anterior insula is composed of three to five short gyri, and the posterior insula is composed of two long gyri. These gyri course radially from the limen insulae in a posterosuperior direction. The limen insulae, a slightly raised area overlying the uncinate fasciculus and the lateral border of the anterior perforated substance, marks the junction of the sphenoidal and insular compartments of the sylvian fissure, and the division between the M1 and M2 segments of the middle cerebral artery (MCA), where the artery turns upward. The insula is separated from the sylvian surfaces of the frontal, parietal, and temporal lobes by the limiting sulcus (circular sulcus).

The central core is situated between the insula and the midline, and is composed of the basal ganglia (putamen, globus pallidus, and caudate nucleus); thalamus; fornix; internal, external, and extreme capsules; and claustrum (Fig. 15.1b). The central core is attached to the rest of the hemisphere by an anterior and posterior isthmus. All information passing between the cortex and the brainstem and spinal cord is relayed in or carried by fibers passing through the central core.

Arteries

The central core and insula are supplied by perforating arteries: small end-arteries that terminate in critical deep structures (Fig. 15.2). Although enlarged cortical feeders to AVMs appear most threatening, they are superficial and often easy to identify, cauterize, and control. In contrast, small perforators that are often overlooked angiographically are deep and difficult to cauterize; they traverse vital white matter tracts, persistently supply the nidus long after the cortical feeders are interrupted, and are accessible only after arriving at the last margin of the AVM. Therefore, they warrant special respect.

The lateral lenticulostriate arteries (lLSA) are the MCA’s perforators. On average, 10 perforators originate from the M1 segment along its superior-posterior surface proximal to its bifurcation, although an early bifurcation results in their postbifurcation origin. The lLSA penetrates the brain at the anterior perforated substance, passes through the putamen, and supplies the upper part of the internal capsule, globus pallidus, and caudate nucleus (head and body).

The medial lenticulostriate arteries (mLSA) are the anterior cerebral artery’s (ACA) perforators. On average, eight perforators arise from the A1 segment, concentrated more proximally (laterally) than distally (medially). The mLSA enters the anterior perforated substance to supply the suprachiasmatic part of the hypothalamus and third ventricle, as well as the dorsal surfaces of the optic chiasm, nerve, and tract. The recurrent artery of Heubner (RAH) is the most medial mLSA, originating from the A1-A2 ACA junction directly lateral to the anterior communicating artery (ACoA) and slightly on the A2 side. It doubles back on itself, paralleling the A1 segment and coursing above the internal carotid artery (ICA) terminus and M1 MCA to the proximal sylvian fissure. It enters the anterior perforated substance with other lLSAs to supply the head of caudate nucleus and adjacent internal capsule, and may also supply the anterior putamen and globus pallidus.

Insular perforators (InsPs) are poorly described in normal anatomic specimens. As is often the case, arteries that are insignificant in the absence of arteriovenous pathology become significant in the presence of such pathology. The InsP supplies AVMs in the sylvian fissure, insula, and lateral basal ganglia. It arises from the M2 segment distal to the limen insulae, which differentiates it from the lLSA arising from the M1 segment. The InsP ascends with M2 stem arteries before penetrating the insular cortex and central core laterally, whereas the lLSA penetrates the central core inferiorly.

The deep venous system collects from veins in the basal cisterns and ventricles, which were discussed in Chapter 14. Important veins include the lateral ones draining the ventricular surface of the central core (Fig. 15.3): the anterior and posterior caudate vein (CauV) draining the caudate nucleus and terminating in ThaStrV; ThaStrV coursing in the striothalamic sulcus between the caudate nucleus and thalamus; the internal cerebral vein (ICV), a paired vein running in the velum interpositum from the foramen of Monro (FoM) to the vein of Galen (VoG); the VoG, which collects from the two ICVs, two basal veins of Rosenthal (BVRs), and the precentral cerebellar vein; and lateral atrial vein (AtrV), which drains the lateral wall of the atrium, posterior thalamus, and caudate body, and then passes through the choroidal fissure to reach the BVR in the ambient or quadrigeminal cisterns. The insula is drained by insular veins, which collect in DeepSylV and the BVR.

Four Deep AVM Subtypes

Deep AVM subtypes include the pure sylvian, insular, basal ganglial, and thalamic AVMs (Fig. 15.4). The pure sylvian AVM, as introduced by Sugita in his classification of AVMs in the sylvian fissure, is located in the fissure without a parenchymal base on the frontal, temporal, or insular cortex (Fig. 15.5). Unlike most other AVMs that are based in brain tissue, pure sylvian AVMs are entirely in the subarachnoid space. The AVM splays the fissure, displacing the superior temporal gyrus down on the temporal side and the precentral gyrus, pars opercularis, and pars triangularis up on the frontal side. There are few other such AVMs whose parenchymal planes are replaced by arachnoidal planes: VoG AVMs, pial brainstem AVMs, and some ventricular AVMs. Pure sylvian AVMs are particularly clean because the dissection is subarachnoid without pial or parenchymal transgression. Furthermore, the location is superficial with excellent exposure. Pure sylvian AVMs are supplied by MCA stem arteries arising from both superior and inferior trunks along their M2 and M3 segments. The nidus resides laterally in the operculum, which situates feeding MCA branches deep to the nidus. Feeders are typically large terminal arteries with high-flow intranidal shunts, which frequently enlarge draining veins into varices. SupSylV and DeepSylV provide drainage, with superficial veins more dominant than deep veins. The sylvian AVMs that do not respect the opercular surfaces of the frontal lobe, temporal lobe, or insula are categorized as sylvian frontal, sylvian temporal, or insular AVMs, respectively. Pure sylvian AVMs were the least common of the deep AVMs (14%), which attests more to their rarity than their operability.

Insular AVMs sit in the limen insulae, short gyri, and long gyri on the insular surface, but lateral to the basal ganglial structures and respectful of the claustrum (Fig. 15.6). Insular AVMs were included in Sugita’s classification of sylvian fissure AVMs and described as deep sylvian AVMs. Insular AVMs were the most common of the deep AVM in my practice, accounting for nearly half (45%) of those treated surgically. The M2 segments supply insular AVMs and course above or lateral to the nidus, requiring the resection to proceed between these arteries. Feeders are large stem arteries and the InsP. Sylvian veins drain these AVMs, with DeepSylV more dominant than SupSylV. Although the role of the insular cortex in speech processing and in conduction between Wernicke’s and Broca’s areas is unclear, it is considered non-eloquent. However, insular AVM exposure in the dominant hemisphere requires dissection adjacent and deep to speech areas in both the frontal and temporal lobes.

The Basal Ganglial AVM

The basal ganglia AVM is deep to the insular cortex in the putamen (Fig. 15.7), globus pallidus, anterior limb of the internal capsule, or caudate nucleus (Fig. 15.8). It sits lateral to the posterior limb of the internal capsule, whereas the thalamic AVM sits medial to the posterior limb. Basal ganglial AVMs have no cortical representation whatsoever and can be reached only laterally through a nonanatomic, transcortical route created either surgically or by hemorrhage. Consequently, basal ganglial AVMs located laterally in the putamen are the most favorable for resection (lateral variant). Some located in the caudate head can be reached medially through a transependymal route through the lateral ventricle (medial variant). The AVMs in other basal ganglial locations are less favorable for surgery. Lateral basal ganglial AVMs are deeper than insular AVMs and are fed by the InsP and lLSA rather than MCA stem arteries. Medial basal ganglial AVMs receive inputs from the mLSA and RAH. Drainage collects in the deep system via DeepSlyV (lateral variant) or CauV and ThaStrV (medial variant). Basal ganglial circuits are eloquent, and proximity to the internal capsule makes these AVMs dangerous.

The Thalamic AVM

Together with the hypothalamus and brainstem, the thalamus is one of the inviolable brain structures that inspires caution. Compelling indications are needed to operate on a thalamic AVM: hemorrhage, significant preexisting deficits, failure of stereotactic radiosurgery, and young age. Thalamus does not tolerate much transgression, and operable AVMs must be small and superficially located on surgically accessible surfaces. Two such surfaces are (1) the superior thalamic surface that forms the floor of the ventricular body, behind the FoM, between the body of the fornix and the body of the caudate nucleus, and deep to the choroid plexus (superior variant, Fig. 15.9); and (2) the medial thalamic surface that forms the lateral wall of the third ventricle deep to the FoM (medial variant, Fig. 15.10). These surfaces are accessible through transcallosal and transcallosal-transchoroidal fissure approaches, respectively. Importantly, AVMs in these entry zones avoid the medial knee of internal capsule. Thalamic AVMs are supplied from below by AntThaP (from PCoA) and PosThaP (from P1 PCA), and from above by lPChA and mPChA. Thalamic AVMs on the superior wall drain ventricularly to the ICV, whereas medial wall drain cisternally to the BVR.

Resection Strategies for Deep AVMs

Pure sylvian AVMs are exposed with a pterional craniotomy and transsylvian approach (Fig. 15.11). The patient is positioned supine with the head turned 20 to 30 degrees away from the AVM and extended 20 degrees, as for an MCA aneurysm, allowing the frontal and temporal lobes to fall naturally to either side of the fissure like pages in a book resting on its binding. The scalp incision and craniotomy extend around the posterior AVM margin, which might require a hairline incision and standard pterional craniotomy for anterior AVMs and a question mark incision and additional parietal/posterior temporal expansion for posterior AVMs (step 1). Pure sylvian AVMs are exposed and circumdissected in the subarachnoid phase of dissection without pial, parenchymal, or ependymal dissection. Sylvian fissure arachnoid is incised below the pars triangularis where the distal fissure is widest, SupSylV is mobilized to the temporal side of the fissure, and the fissure is split from distal to proximal (step 2). Drainage through an enlarged or variceal SupSylV remains centered over the nidus throughout the dissection (step 3). Supply originates from the insular M2 and opercular M3 segments of MCA stem arteries and from both superior and inferior trunks (step 4). These feeding arteries are situated underneath the nidus on both the frontal and temporal sides, forming an anteromedial front (step 5). Sylvian arteries are a mixture of terminal feeding arteries, transit arteries, and bystander arteries. High-flow terminal feeders are identified in the proximal fissure on the inferomedial AVM margin as large pipes that frequently require occlusion with aneurysm clips rather than cautery. Transit arteries require skeletonization in a distal-to-proximal direction to interrupt their smaller nidal inputs and also preserve cortical arteries that continue en passage. Uninvolved bystander arteries are separated from the nidus and mobilized temporally or frontally. Meticulous arachnoidal dissection in the sylvian cistern maintains pial integrity and no parenchymal transgression is needed for circumdissection (step 6). Deep dissection exposes the full course of the M2 and M3 stem arteries, DeepSylV drainage, and insula cortex (step 7). Pure sylvian AVMs are extraparenchymal and therefore non-eloquent, but are adjacent to speech areas in the dominant frontal and temporal lobes (Figs. 15.12 and 15.13).

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Pial Dissection Draining Veins Parenchymal Dissection Patient Selection Temporal Arteriovenous Malformations Cerebellar Arteriovenous Malformations

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