Surgery of Basal Ganglia, Thalamic, and Brainstem Arteriovenous Malformations

17 Surgery of Basal Ganglia, Thalamic, and Brainstem Arteriovenous Malformations

Venkatesh S. Madhugiri, Mario Teo, and Gary K. Steinberg

Abstract

Arteriovenous malformations (AVMs) of the basal ganglia, thalamus, and brainstem are among the most challenging lesions neurosurgeons are called upon to treat. These deep-seated AVMs account for 2 to 12% of all intracranial AVMs, have a higher risk of hemorrhage than more superficial lesions, and frequently require complex multimodal management paradigms. Endovascular embolization is usually a prelude to surgery. Residual lesion after endovascular therapy and/or surgery can be managed by radiosurgery. The optimal surgical approach is based on the location of the lesion and its proximity to an ependymal or cortical surface. For AVMs of the basal ganglia and thalamus, six main surgical approaches are used individually or in combination: (1) frontal interhemispheric transcallosal, (2) parietal interhemispheric transcallosal, (3) occipital transtentorial infrasplenial, (4) supracerebellar infratentorial, (5) transsylvian, and (6) transcortical. For brainstem AVMs, the approaches are based on six described anatomic locations of the lesions using the safe entry zone, and we often favor the “occlusion in situ” technique. Pial brainstem AVMs can be safely excised or surgically obliterated, whereas parenchymal brainstem AVMs are best managed by nonsurgical means. Furthermore, several intraoperative adjuncts are useful for the safe resection of these deep-seated lesions, including neuronavigation, mild hypothermia, strict control of the mean arterial pressure (also postoperatively), electrophysiological monitoring, and ICG or digital subtraction angiography..

Keywords: AVM, brainstem, basal ganglia, thalamic, endovascular embolization, hemorrhage, microsurgery, radiosurgery

Key Points

Deep-seated arteriovenous malformations (AVMs) usually have a higher risk of hemorrhage than more superficial lesions.
No single treatment modality can usually achieve a complete cure. Endovascular embolization is frequently a prelude to surgery or radiosurgery. Residual AVM after endovascular therapy and/or surgery can be managed by radiosurgery.
Several preoperative and intraoperative adjuncts such as neuronavigation, controlled mild hypothermia, strict control over the mean arterial pressure during and after surgery, electrophysiology, ICG and intraoperative angiography are required for the safe resection of these lesions.
Surgical approach is tailored to the location of the lesion and its proximity to an ependymal or pial surface.
Pial brainstem AVMs can be safely excised, whereas parenchymal brainstem AVMs are best managed by nonsurgical means.

17.1 Introduction

Arteriovenous malformations (AVMs) of the basal ganglia, thalamus, and brainstem are among the most challenging lesions that neurosurgeons are called upon to treat. These relatively rare lesions usually require complex multimodal management paradigms.¹ AVMs involving the basal ganglia and thalamus comprise about 2 to 12% of all AVMs, whereas brainstem lesions are rarer still and probably account for 2 to 6% of all intracranial AVMs.²^,³ The mortality rate for a first hemorrhage from all AVMs has been reported to be about 10%, and about 13 and 20% for subsequent rebleeds.⁴ The annual risk of hemorrhage is 2 to 3% per year, except in the first year after a bleed when the chance of rebleed is approximately 6%. There is some evidence to suggest that deep and centrally located lesions, such as those in the basal ganglia, thalamus, and brainstem, have a more aggressive course than AVMs in more superficial locations in the brain.¹ In one large series, 71.9% of these patients presented with hemorrhage, with an annual rebleed rate of 11.4% during a 6.6-year follow-up.⁵ Our Stanford series of 96 basal ganglia and thalamic AVM patients (69% presenting with hemorrhage) demonstrated a rebleed rate of 9.6%/year after diagnosis, but before any treatment. This is a worrisome issue, given that a bleed in these areas can be devastating—hemorrhage in patients with deep AVMs can not only lead to profound motor and sensory deficits but also to cognitive and memory disorders.⁶ Only about a fifth (21.9%) of patients who are diagnosed with an AVM in the basal ganglia or thalamus are likely to be neurologically intact at the time of their original presentation, irrespective of whether they presented with a bleed or not.⁷ Brainstem AVMs have an equally high risk of bleeding—up to 88.5% of patients presented with hemorrhage in some series. Brainstem hemorrhage can have devastating consequences, including immediate death or deep coma in up to 40% of patients.⁸^,⁹ Hemorrhage from these lesions could easily extend into the ventricles and obstruct the cerebrospinal fluid (CSF) pathways. Management of the lesion itself would then be complicated with the addition of hydrocephalus. Indeed, the presence of hydrocephalus in patients who present with a ruptured AVM could portend a poorer prognosis.¹⁰

There are several issues to be considered while managing these lesions. The first would be to recognize patterns of clinical presentation in those patients who do not present with hemorrhage so that early diagnosis and treatment of unruptured lesions can be achieved. Various series have reported rates of presentation with hemorrhage of 70 to 88%.¹^,⁷ Other clinical symptoms and signs include headache in 27.1%, neurological deficits including hemiparesis in 61.5%, visual field defects in 12.5%, dysphasia in 14.6%, and seizures in 13.5%.⁷ The second issue would be to formulate effective multimodal management strategies. Not only do these patients present with more severe deficits, but surgery outcomes are not as good as for AVMs in other locations.¹¹ The availability of endovascular (embolization) therapy (EVT) and radiosurgery has made it possible to cure some of these lesions. However, no single technique can usually achieve a cure when applied in isolation.¹ In up to 16% of patients in our series of deep AVMs, all three modalities of treatment were invoked.² In the Stanford AVM series, only 4 of 124 patients (3.2%) with basal ganglia/thalamic AVMs were completely cured without surgery—1 with EVT and 3 with a combination of EVT and radiosurgery.²

EVT is usually performed as a prelude to surgery to reduce the vascularity of the lesion. Endovascular embolization prior to surgical excision is not always feasible because many of these lesions derive their blood supply from deep perforating arteries, including the lenticulostriate arteries, insular perforators, thalamoperforators, and anterior and posterior choroidal arteries. The long, short, and circumflex brainstem perforators that would ultimately supply intraparenchymal brainstem AVMs are difficult to embolize as well. In one large series, only 41% of these lesions could be effectively embolized prior to surgery.¹² Other series have reported complete obliteration rates of 14.5 to 20% with EVT alone.¹³^,¹⁴

Radiosurgery is a viable option for basal ganglia and thalamic AVMs, especially for those lesions that have not bled. A cure can be effected after a single session of radiosurgery in as many as 61.9% of patients. In one series, the annual risk of hemorrhage after radiosurgery was 9.5% in the first year, 4.7% in the second year, and 0% thereafter.¹⁵ Radiosurgery does not confer complete protection from hemorrhage until the AVM is completely obliterated. In a large radiosurgery series, 88% of patients presented with hemorrhage. After radiosurgery, 14.3% experienced bleeds during follow-up, with a mortality of 50%. This is an important factor to consider when recommending radiosurgery for these lesions. Radiosurgery is a good option for brainstem lesions as well, and the efficacy seems undiminished because of the location of these lesions in the posterior fossa.¹⁶

Although these basal ganglia, thalamic, and brainstem lesions are deep seated and difficult to access, there are definite indications for microsurgery. One indication is to evacuate large hematomas that could cause herniation. AVMs that are not completely obliterated after multiple sessions of radiosurgery or embolization are another potential indication for surgery. Lesions that abut a ventricular wall could potentially be accessed more easily than those that are completely intraparenchymal. This chapter discusses the surgical strategies to tackle these lesions.

17.2 Patient Selection

As already discussed, hemorrhage rates for patients with basal ganglionic and thalamic AVMs could be significantly higher than those with lesions in other locations. In a review of untreated patients with more than 500 patient-years of follow-up (who were ultimately referred to Stanford for evaluation), the pretreatment annual rupture rate was 9.6% per year. Periventricular AVM location and deep venous drainage have been identified as independent risk factors for hemorrhage in large natural history studies, including one from Finland.¹⁷ A history of previous hemorrhages correlates with bleed recurrence in the AVMs of the thalamus and basal ganglia.⁷^,¹⁷^,¹⁸ Hemorrhage from a basal ganglia or thalamic AVM also carries a risk of serious morbidity, with up to 85% of post-bleed patients developing hemiparesis or hemiplegia. The higher risk of hemorrhage and greater morbidity from hemorrhage should be factored into the decision as to whether to treat basal ganglia and thalamic AVMs. Given the high rates of hemorrhage and the devastating consequences thereof, observation may not be a reasonable option.

Brainstem AVMs also have annual hemorrhage rates as high as 15 to 17.5%, which makes observation and follow-up difficult to justify as a management strategy.¹⁹^,²⁰ Hemorrhage from brainstem AVMs is associated with a poor prognosis, with death in as many as one-third of treated and two-thirds of untreated patients.²¹^,²² The Lawton-Young AVM grading system incorporates patient age (< 20, 20–40 years, or > 40 years), hemorrhagic presentation (ruptured vs. unruptured), and compactness of the nidus (compact vs. diffuse) in addition to the variables in the Spetzler-Martin grading system.²³ This scale could be used as a part of the decision-making process as it scores patients with prior hemorrhage higher—these are also the patients who would require immediate management rather than observation.

Poor candidates for surgery would be patients with severe comorbidities, elderly patients, and patients with devastating neurological deficits. Patients with lesions located within the posterior limb of the internal capsule should receive treatment with non-microsurgical techniques because of the high risk of permanent deficits. In patients with asymptomatic AVMs, the risk of surgical morbidity should be carefully weighed against the natural history of the lesion and patient-specific factors. Patients presenting with hemorrhage are known to have a worse natural history and poorer outcomes after rehemorrhage; thus, carefully tailored low morbidity treatments with a goal of AVM obliteration can decrease future hemorrhage risk and the associated morbidity.

17.3 Imaging and Embolization

Preoperative high-quality magnetic resonance imaging (MRI) and digital subtraction angiography (DSA) are essential to understanding an AVM’s angioarchitecture and cerebral location. The presence of associated aneurysms, high flow shunts, and venous varices should be noted. In some cases, preoperative MR tractography can be useful to localize the traversing tracts and understand their disposition relative to the nidus, aid in surgical approach selection, and enhance intraoperative neuronavigation. We highly recommend that a navigation protocol MRI with an MR angiogram be performed the day prior to surgery to guide the approach to and resection of deep AVMs. CISS-3D or FIESTA sequences could also be of use in tracing the feeding vessels and draining veins. Thalamic and basal ganglionic AVMs are generally fed by the medial and lateral lenticulostriate arteries, recurrent arteries of Heubner, thalamogeniculate arteries, thalamoperforating arteries, and anterior and posterior choroidal arteries. Almost all AVMs in the basal ganglia and thalamus have deep venous drainage. In patients with AVMs amenable to embolization, we recommend staged embolizations spaced at least 1 week apart. We never attempt to embolize more than 30% of the AVM at any session because more aggressive embolization can cause swelling and hemorrhage. It should be borne in mind that embolization, even as a prelude to surgery, is not entirely without risk. In a series of supratentorial AVMs treated with partial or complete embolization, 6.9% of patients developed permanent neurologic deficits after embolization. The risk factors for postprocedure deterioration were identified as location in eloquent areas and exclusive deep venous drainage.²⁴

17.4 Anesthetic Technique and Electrophysiology

Surgery is usually performed with the patient under general anesthesia. Several surgeons have reported performing AVM excision with the patient awake. This technique appears to be especially useful to map cortical and subcortical speech areas using intraoperative stimulation.²⁵^,²⁶ The safety that is afforded with the patient awake should be balanced against the tight anesthesia and hemodynamic control that are usually required for AVM excision. The patient’s mean arterial pressure (MAP) should be controlled between 70 and 80mm Hg throughout induction of anesthesia and surgical exposure. MAP should be reduced further to between 60 and 70mm Hg during resection of the AVM through emergence from anesthesia. We also recommend mild hypothermia with a target core temperature of 33 to 34°C achieved via a cooling blanket and/or cold saline infusion via femoral venous catheters. Experimental evidence and some clinical studies have shown mild hypothermia to be protective against cerebral ischemic insults.²⁷ Electrophysiological monitoring and mapping are important tools in the resection of AVMs. The use of continuous bilateral upper and lower somatosensory-evoked potentials (SSEPs) and motor-evoked potentials (MEPs) along with cortical and subcortical mapping can be invaluable in decreasing the risks associated with the surgical and endovascular management of these lesions. We routinely use electrophysiologic monitoring for all patients undergoing microsurgical excision of deep AVMs.

17.5 Surgical Techniques

Adequate exposure is critical to resecting deep vascular malformations. Virtual reality-based software may be especially useful in the preoperative planning of the stepwise surgical strategy.²⁸^,²⁹ It is critical to identify the arterial feeders, which form the initial points of attack, early on in the procedure. Their position should be predicted from the preoperative DSA and MRI, and neuronavigation should be used in localizing them intraoperatively. They should then be divided close to the nidus while preserving the draining veins. Several millimeters of a feeding artery should be exposed prior to coagulation or using micro-clips—this is because of the tendency of these feeders to retract into the brain parenchyma once they are cut. The veins are usually arterialized and should not be mistaken for feeding arteries, given inadvertent sacrifice of draining veins early on in the procedure can lead to AVM swelling and rupture. Intraoperative indocyanine green (ICG) angiography and the use of the Charbel Transonic flowmeter, which indicates direction of flow, may be useful in distinguishing arteries from arterialized veins.²⁹ Microsurgical resection is performed under high-power magnification with very fine irrigating bipolar coagulation forceps or the Spetzler-Malis nonstick bipolar, using low coagulation power to limit the spread of current to surrounding brain tissue.³⁰ The nidus is then dissected from the surrounding brain as the surgeon looks for gliotic and hemosiderin-stained brain as a plane. The plane of dissection should remain as close to the periphery of the nidus as possible to minimize the risk of injuring normal brain. However, occasionally “dirty coagulation” may need to be performed of the deep, small, difficult vessels inside apparently normal brain around the AVM.³¹ One group recommends the neuroendoscope as a useful tool to develop the plane of dissection, especially in those AVMs that abut the ventricular surface.³² The final step is to divide the draining veins. Intraoperative angiography is often helpful to confirm the excision of the nidus while operating on these complex lesions.³³ In one series, 22.22% of patients had a residual nidus on intraoperative angiography that required further excision.³⁴ Several series also report the use of ICG angiography to confirm excision, but we do not consider this as valuable as catheter angiography because the dye does not visualize deeper aspects of the AVM.²⁹

Careful hemostasis should be achieved and confirmed by gently raising the MAP to normal levels as well as by using the Valsalva maneuver before the dura is closed. The surgical bed should be lined with Surgicel (Ethicon, Inc., Somerville, NJ) to induce hemostasis of small vessels. If the ventricle was entered, a ventricular catheter is often placed prophylactically. The dura is then closed primarily or with the aid of a dural substitute. We use 4–0 braided nylon suture for dural closure. The bone is replaced with titanium plates and screws, the galea is closed with 2–0 absorbable sutures, and staples are placed in the skin.

17.5.1 Surgery for Basal Ganglionic and Thalamic AVMs

There are six main surgical approaches used individually or in combination for AVMs of the basal ganglia and thalamus, depending on lesion location: (1) frontal interhemispheric transcallosal, (2) parietal interhemispheric transcallosal, (3) occipital transtentorial infrasplenial, (4) supracerebellar infratentorial, (5) transsylvian, and (6) transcortical (frontal or parietal). The point of closest presentation of the lesion to a ventricular or pial surface influences the surgical trajectory as does the proximity of a hematoma cavity to these surfaces. We may use a ventriculostomy or lumbar drain for brain relaxation before positioning. However, this is not necessary if an intraventricular approach is utilized, given that CSF can be drained directly with the opening of the ventricle. Additional steps to induce brain relaxation include hyperventilation, diuresis, or both. The groin should also be prepared for possible intraoperative angiography.

Interhemispheric Transcallosal Approach—Frontal and Parietal

AVMs that present to a ventricular surface are best exposed via a transcallosal route (► Fig. 17.1). Lesions of the medial aspect of the caudate are best approached via an anterior transcallosal approach and those of the posterior medial thalamus and pulvinar via a posterior transcallosal approach. For the frontal approach, the patient is positioned supine with the head slightly elevated above the heart and flexed 20 to 30 degrees. Alternatively, an ipsilateral side-down, lateral position could be used so that the frontal lobe falls away from the falx under the influence of gravity. A paramedian trapdoor incision is made on the side of the AVM. We usually place two-thirds of the flap anterior and one-third of the flap posterior to the coronal suture. For the parietal approach, the patient is placed in a park-bench position and the anterior margin of the craniotomy is posterior to the postcentral gyrus. The bone flap should be planned after reviewing the coronal and sagittal MRI sequences so as to locate the positions of the draining veins into the sagittal sinus. The bone flap is made large enough in the anterior-posterior direction to allow preservation of these cortical draining veins. The bone flap is usually taken across the midline, exposing the superior sagittal sinus. The dura is incised based on the sinus and tacked up, giving a wider access to the interhemispheric fissure. When large cortical draining veins prevent exposure from one side, a dural incision and approach may be performed from the contralateral side. Although it is thought that the division of one cortical draining vein may not lead to a significant problem, this is not necessarily true. The size and drainage territory of the sacrificed vein, the development of the Sylvian system, and collateral drainage all determine if venous infarction would occur or not.³⁵

Fig. 17.1 A Spetzler-Martin grade III thalamic arteriovenous malformation (AVM) treated by multimodal management. The patient presented with a massive intraventricular hemorrhage. He underwent embolization of some of the posterior cerebral artery feeders followed by partial surgical resection of the nidus and CyberKnife to the residual lesion. (a) Axial T2-weighted image showing an AVM in the left thalamus with hemorrhage extending into the lateral ventricles. (b) Anteroposterior view of an angiography showing the nidus, supplied predominantly by the left posterior cerebral artery and draining into the vein of Galen. (c,d) Posttreatment angiography. The anteroposterior (c) and lateral (d) views show no residual nidus.

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