Intraventricular and Deep Arteriovenous Malformations

Patient Selection

Choosing observation, microsurgical resection, focused irradiation, embolization, or some combination of these as the recommended management for deeply located arteriovenous malformations (AVMs) requires understanding of the risks and benefits of each of these pathways as well as of the natural history of the AVM. The risk for hemorrhage is 1 to 3% for unruptured AVM and 4 to 6% for AVM presenting with recent rupture. ¹^, ² Associated aneurysms and deep venous drainage system may also increase the hemorrhage risk for untreated unruptured AVM. Focused irradiation offers the benefit of avoiding the complex surgery necessary for deeply located AVMs but needs to take into account the latency period between treatment and obliteration during which time the natural history of rupture prevails.

Surgery has a high immediate cure rate but carries substantial risk for deep AVMs. Surgical risk depends on the size, location, and compactness of the nidus. ³^, ⁴^, ⁵^, ⁶ Most deep AVMs recommended for surgery are either Spetzler–Ponce class A or B. ⁶ There is a major difference in the risk of surgery between these two classes. Class A have a risk of permanent new neurological deficit less than 5% whereas it may be 10 to 24% for class B cases. ⁶^, ⁷^, ⁸ The risk benefit for class C may favor nonoperative management ( ▶ Fig. 25.1).

Fig. 25.1 Arteriovenous malformations (AVMs) chosen not to operate on by the authors. (a) Right hemispheric Spetzler–Martin grade 5 AVM. (b) Anteroposterior and (c) lateral digital subtraction angiogram of a right basal ganglia grade 5 AVM with lenticulostriate involvement.

Embolization of the AVM as a single modality, or as a precursor to surgery or focused irradiation, is highly nuanced. ⁹ The authors of this chapter describe surgery without preoperative embolization.

25.2 Preoperative Preparation

25.2.1 Imaging

Catheter angiography with three-dimensional reconstructions and selective catheterization of feeding arteries, when additional information is required, are the gold standard for the evaluation and planning for surgical resection. Angiography accurately identifies arterial feeders and their location, diameter, length, and tortuosity as well as intranidal or arterial feeding aneurysms ( ▶ Fig. 25.2, ▶ Fig. 25.3). This information enables an estimate of the natural history of the lesion, as well as helps to prepare the surgeon for where feeders will be found during surgery.

Fig. 25.2 Magnetic resonance imaging and catheter angiography of an arteriovenous malformation approached best through the floor of the left lateral ventricle.

Fig. 25.3 Catheter angiography of an arteriovenous malformation (AVM) of the corpus callosum, caudate, hypothalamus, and third ventricle. This was approached through an anterior transcallosal incision having exposed a long segment of the anterior cerebral artery before callosotomy and AVM resection.

Magnetic resonance imaging (MRI), potentially functional and diffusion tensor imaging, allows a better appreciation of the relation of the nidus to the surrounding brain and are useful for calculating AVM size, the relationship to the ventricles, sulci surface presentation of the lesion, and location of eloquent cortex and white matter ( ▶ Fig. 25.2).

Functional brain rarely exists within the interstices of the AVM. Therefore, if a marginal resection is achieved, it can be assumed, in most cases, that critically functioning brain can be preserved. Neurological deficits may develop in rare cases where functional brain exists within the AVM but more commonly when an artery “en passage” is occluded along with the AVM or the brain adjacent to the AVM is injured, usually in attempts to control bleeding from deep feeding arteries.

25.3 Operative Procedure

General principles for removal of deep AVMs are:

Craniotomies need to provide optimum exposure of the AVM in order to minimize retraction and maximize the ability to identify and access proximal arteries and venous drainage. For deep locations, consideration needs to be made of optimizing access through a fissure and sulcus. Insular AVMs require an exposure that allows the entire sylvian fissure to be opened. Medial frontal, parietal and occipital AVMs can be maximally exposed by operating on either side of the superior sagittal sinus with the contralateral approach through the falx cerebri for the most medial and the most lateral aspect of the AVM. Intermediately located AVMs may be more readily accessed by the ipsilateral approach. In this case, having the superior sagittal sinus perpendicular to the ground facilitates exposure. For lateral ventricular AVM, approaching the relevant lateral ventricle through a contralateral side assists in accessing the most lateral aspect of the AVM (Video 25.1).
Feeding arteries need to be dissected proximal as well as distal to all branches to the AVM. Preserving the distal arterial supply to normal brain is best achieved proceeding from distal to proximal, ligating and dividing terminal arteries supplying the AVM after determining the distal normal arterial supply. This strategy minimizes the potential inadvertent mistake of removing the normal distal artery (Video 25.2, ▶ Fig. 25.3).
Temporary arterial clips applied to feeders at a distance from the AVM provide regional hypotension within the AVM, provided that almost all feeding arteries are controlled (ensuring that the venous drainage is not impeded). This strategy improves the safety of dissection on the AVM margin.
Retraction should be minimized but is unlikely to be avoided in deeply placed AVM. Retraction of the brain may exacerbate ischemia. Light and limited retraction of the AVM is safe providing that venous outflow is not impeded. Impeding the venous outflow will increase the tension within the AVM.
Securing arteries by bipolar is made difficult by the thin walls of small feeding arteries (relative to the vessel radius). This makes coagulation difficult with bursting of the vessels if not performed carefully with clean bipolar tips at coagulation settings lower than normally employed. In addition, the use of microclips (e.g., as invented by Sundt) to arrest flow can assist either with diathermy or as the principle ligating agent. ¹⁰ Some surgeons prefer irrigating bipolars or disposable bipolar forceps. An additional technique suitable for some vessels includes incorporating adjacent brain with broad bipolar blades to spread the current and incorporate more material to assist with sealing vessels (Video 25.3). ¹¹
Securing all arterial input before venous drainage is compromised is critical. In order to achieve this without causing the most distal AVM becoming tense and easily ruptured is assisted by first securing the accessible superficial feeding arteries followed by a partial and limited AVM marginal arc dissection to the deepest component of the AVM (including entry into the ventricles if the AVM juxtaposes the ventricle) to secure arteries to the deep nose cone. This differs from the normal planned circumferential spiral, in a corkscrew approach, achieving an even depth of dissection on the margin of the lesion. This corkscrew circumferential dissection is not recommended until after the deep feeders are controlled. This is because the venous component of the AVM is located on the surface of the AVM and in the process of corkscrewing the dissection, this superficial venous drainage, internal to the AVM, may be increasingly compromised with preservation of a deep arterial contribution to the nose cone. Therefore, securing the deep feeding arterial supply should precede a circumferentially deepening dissection of the resection margin (Video 25.4).
Small arterialized vessels must be followed for a short distance into the white matter during the corkscrew circumferential dissection before a decision to ligate these vessels is made. This is because it is not easily possible to distinguish small feeding arteries from arterialized venous loops that leave and then rejoin the AVM. The cumulative ligation of venous loops will progressively impede venous drainage from the depth of the AVM. The final nose cone then may become very tense if its arterial input has not been secured. Therefore, the venous loops should be left unligated and only the infrequent arterial input ligated and divided.
Before ligation and division of the main draining vein is attempted, the resected AVM should be delivered from the resection bed with the small umbilical attachment of the draining vein remaining.
Inspection of the resection bed should find absolutely no arterialized bleeding. Any bleeding should raise the possibility of retained AVM that may lead to catastrophic postoperative hemorrhage. It is important not to stress test the security of hemostasis by raising blood pressure during the surgery. Any area in the bed of the AVM with arterialized bleeding must be explored. Irrespective of whether this bleeding is due to retained AVM or not, the small vessels responsible for persistent bleeding have not the capacity to constrict due to their minimal muscular wall. Bleeding needs to be specifically surgically arrested rather than allow time to pass for and anticipated arterial vasoconstriction response for control.
In cases where there is meningeal supply to the AVM, it is important that the dura and brain not be retracted apart as the bridging artery may tear. An indirect approach to these feeding arteries within the dura is appropriate by creating an island of dura and leaving this on the brain over the AVM. The tentorium cerebelli or the falx cerebri can be incised at a considerable distance from the AVM securing the blood supply (e.g., division of the tentorium from lateral to medial will secure the meningeal arterial supply from the carotid artery or opening of the falx from a contralateral approach at a distance from the nidus can deal with feeders entering from the falx).

Another important consideration is the impact of the dissection through the brain when obtaining access to the deep feeders. Thought needs to be given not only to the function of the tissue to be divided (such as the association fibers) but also to whether tandem lesions will be created. Two tandem lesions that need consideration include whether the dominant visual cortex is damaged if the splenium is intended to be divided, because this would render the language cortex to be disconnected from functional visual cortex. The other is whether previous external ventricular drain insertion may have injured one or the other of the fornices when one is planning to enter contralateral memory systems such as the fornix, hypothalamus, and thalamus. Inadvertent bilateral injury may have catastrophic effects upon memory function.

One final point concerns previously inoperable AVMs in eloquent areas that are selected for surgical intervention. In cases of massive hemorrhage or infarction that induce permanent focal neurological deficit or are life threatening, direct surgical corridors through overlying eloquent cortex may be indicated and be feasible without creating additional neurological deficits ( ▶ Fig. 25.4).

Fig. 25.4 (a) T1-weighted magnetic resonance imaging showing acute hemorrhage from a deep right arteriovenous malformation (AVM). (b) Computed tomography showing massive hemorrhage secondary to a deep right AVM. This mandated surgical extirpation. (c) The surgical corridor through the cortex overlying the AVM can be seen.

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