Surgical and Radiosurgical Management of Giant Arteriovenous Malformations

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CHAPTER 389 Surgical and Radiosurgical Management of Giant Arteriovenous Malformations

Successful treatment of arteriovenous malformations (AVMs) remains one of the more challenging problems faced by neurosurgeons. Giant AVMs represent a rare, but excessively difficult group of AVMs that are often associated with higher treatment morbidity and mortality than their smaller counterparts. The standard definition of a giant AVM is a high-flow, angiographically visible vascular malformation that is greater than 6 cm in maximum diameter. The size alone results in a Spetzler-Martin grade of at least III, and most of these giant AVMs are classified as Spetzler-Martin grade IV or V.¹ The size of these giant AVMs almost invariably results in at least a portion of the malformations being located within or immediately adjacent to eloquent regions of the brain, and these lesions often have both deep and superficial venous drainage. Giant AVMs frequently have an arterial supply from multiple vascular distributions, from the anterior as well as the posterior circulation, and in many cases the arterial supply is bilateral.

Many of these giant AVMs were previously considered “untreatable” by neurosurgeons because of their size. However, over the past 2 decades neurosurgeons have developed novel approaches that allow treatment of these lesions with acceptable risk. The use of microinstrumentation and the neurosurgical microscope, along with the aid of image-guided navigation, electrophysiologic monitoring, hypothermia, and preoperative embolization, have enabled neurosurgeons to resect some of these lesions safely. Furthermore, stereotactic radiosurgery has allowed treatment of many giant AVMs, either by decreasing the size of the nidus after radiosurgery and facilitating resection of a smaller AVM or by treating residual AVM after surgery or embolization. Optimal management of these giant AVMs must therefore include a detailed understanding of the hemodynamics and anatomy of each particular vascular malformation, as well as familiarity with the various methods of AVM treatment.

Clinical Findings/Preoperative Evaluation

Symptoms

The size of giant AVMs and the large amount of arteriovenous shunting within these lesions often result in symptoms unique from those with smaller AVMs. Small vascular malformations are typically manifested as headaches,^2,³ seizures,⁴^–⁶ or hemorrhage.⁵^–⁹ Giant AVMs can have any of these symptoms but can also cause transient and progressive neurological dysfunction through cerebrovascular “steal.” The large blood volume shunting through these malformations can result in relative hypoperfusion in the surrounding neurological tissue with subsequent ischemia.¹⁰^–¹³ This is due to lower blood pressure within the arterial feeders of the AVM than in the surrounding brain, which results in preferential shunting of blood to the AVM away from normal brain tissue.

AVMs have initial hemorrhage rates of 2% to 4% and annual rebleeding rates of approximately 4% to 18%.^7,¹⁴^–¹⁷ Mortality from each hemorrhage approximates 10% to 15%,^5,⁸ and up to 50% of patients suffer some form of neurological deficit as a result of bleeding from an AVM.⁹ Some authors believe that larger AVMs have bleeding rates slightly lower than their smaller counterparts.^7,^18,¹⁹ Other studies have shown no consistent relationship between size and risk for hemorrhage,^14,²⁰ and feeding artery pressure (believed to be a risk factor for AVM hemorrhage) did not correlate with AVM size.²¹ However, giant AVMs with components in the basal ganglia, thalamus, and pineal region may be associated with not only a higher hemorrhage rate²² but also increased morbidity if they bleed, with more than 60% of these patients suffering significant morbidity or death from hemorrhage.²³ Angiographic factors that have been shown to correlate with risk for AVM hemorrhage are central venous drainage, periventricular location, and intranidal aneurysms,^24,²⁵ as well as a single draining vein²⁵ and stenotic venous drainage.²⁶ By their size alone, giant AVMs are more likely to have a component of central venous drainage and a portion of the AVM adjacent to or within the ventricle.

Indications for and Contraindications to Surgery

Indications for resection of giant AVMs must consider both the natural history of the AVM and the combined risks associated with multimodality treatment for a particular patient.^27,²⁸ Most angiographically documented giant AVMs are candidates for treatment, particularly if they have hemorrhaged or are causing significant progressive neurological deficits, disabling headaches, or medically intractable seizures. The risk with surgical resection is generally related to AVM size and location and the complexity of arterial feeders and venous drainage,¹ factors that make these giant AVMs a higher risk than smaller AVMs to treat with surgery alone. Larger lesions may require staged surgical resection or multimodality therapy combining microsurgery, embolization, and stereotactic radiosurgery.²⁷^–³⁰ Other factors affecting treatment risk include the patient’s clinical condition and age and surgeon experience.

The location of the giant AVM under consideration significantly affects the risk associated with surgical resection.²⁷^–³² Because of their size, these larger AVMs often involve eloquent cortex, which significantly increases the risk of resection. Resection of giant cortical AVMs may cause motor or sensory deficits (frontal/parietal) or visual field defects (occipital), memory deficits, and changes in cognition and personality (cingulate gyrus and corpus callosum). Treatment of deep portions of giant AVMs within the basal ganglia and thalamus can result in hemiplegia, sensory deficits, dysphasia, and cognitive and memory deficits.^23,^33,³⁴ The clinical condition of the patient also has a bearing on surgical resection, with poor-grade patients usually resulting in a poor outcome.²⁹ Younger patients have a better benefit-to-risk ratio for the treatment of giant AVMs for two reasons. First, the brain of a young patient can better tolerate resection of the vascular malformation and has improved recovery after surgery.³⁵ Second, a younger patient translates into longer AVM-free survival on completion of resection.³⁵ Likewise, patients with a significant mass effect from a hemorrhagic clot resulting from AVM rupture should undergo emergency evacuation of the hemorrhage, with resection of the AVM being reserved for a later date. The timing of resection of giant AVMs is similar to that for other AVMs in that resection should be planned under nonemergency conditions to minimize patient morbidity. Resection of the AVM 4 to 6 weeks after hemorrhage, when the blood is liquefied, may improve the ease of resection.^8,^23,^30,³⁶ In many cases, the hematoma cavity has performed a portion of the dissection around the nidus of the AVM. Furthermore, this short interval allows the patient to achieve stabilization or improvement of any neurological deficits.

Failure of stereotactic radiosurgery and embolization is another indication for surgical resection,^27,^30,³² although in the case of giant AVMs, these treatment modalities are generally used as adjuncts in reducing AVM size before planned microsurgical resection. Most studies indicate that partial obliteration after radiosurgery does not confer protection from AVM rehemorrhage,^23,^27,^29,^33,^37,³⁸ and hence an alternative therapy should be sought for residual AVMs seen more than 3 years after radiosurgical treatment. Embolization is a useful treatment of giant cortical AVMs,³⁹ but it is less useful in the treatment of deeper arterial feeders (thalamoperforating, choroidal, and lenticulostriate arteries) within the basal ganglia and thalamus. These vessels primarily arise from the parent vessels at right angles, have small lumens, and are thus difficult to canulate.^23,^33,³⁴ Nonetheless, in selected cases, embolization has been extremely helpful in partially obliterating even basal ganglia and thalamic arterial feeders.^29,^30,⁴⁰

Contraindications to the treatment of giant AVMs include poor clinical condition of the patient as a result of AVM hemorrhage, medical conditions precluding surgery, and very elderly AVM patients. Frequently, patients in poor neurological condition may improve over time or with minor procedural interventions, such as placement of a ventriculostomy or ventriculoperitoneal shunt for hydrocephalus, and may then be candidates for treatment. Other patients with significant neurological deficits as a result of hemorrhage can make dramatic improvements with time and would therefore qualify for treatment. Patients who have giant AVMs but are asymptomatic or have minimal symptoms are sometimes best observed clinically rather than treated.

Hemodynamics Of Giant Arteriovenous Malformations

All AVMs serve as a shunt between the arterial and venous systems. Pressure within the arterial feeders of AVMs has been shown to be lower than the pressure in normal brain arteries, whereas pressure within the venous channels draining the AVM has been shown to be higher than normal venous pressure. Furthermore, as a result of this low pressure on the arterial side, blood that would normally supply the cortex adjacent to the AVM may preferentially flow to the AVM. This cerebrovascular steal, which may be more pronounced with giant AVMs, is hypothesized to cause ischemic symptoms within the cortex adjacent to the AVM. The arteries within the adjacent cortex respond to this steal phenomenon by dilating their lumen to maintain flow through autoregulation. The extended interval in which these cortical arteries remain dilated results in the loss of their rapid ability to constrict should the blood pressure within these cortical arteries change. When these vessels are subjected to a higher pressure head, as when the low-resistance high-flow giant AVM is removed, they may not have adequate autoregulatory compensation, and edema and hemorrhage in the surrounding brain parenchyma can result. Angiographic characteristics found to be correlated with cerebrovascular steal are angiomatous change, AVM size, and pattern of peripheral venous drainage.⁴¹

The process of impaired autoregulation and hemorrhage from cortical vessels adjacent to an AVM after AVM resection is called normal perfusion pressure breakthrough.⁴² Although this phenomenon is rare, it is believed to occur more frequently in giant AVMs because these malformations shunt a higher volume of blood and thus create more vascular steal from the surrounding cortex.²⁷ AVM features associated with an increased likelihood of normal perfusion pressure breakthrough (other than AVM size) include dilated feeding arteries, poor filling of the surrounding cerebral vasculature on angiograms, clinical symptoms of ischemia from cerebral vascular steal, and physiologic evidence of impaired autoregulation in the brain.^31,⁴³ Normal perfusion pressure breakthrough–associated bleeding can be limited by careful control of blood pressure in the immediate postoperative period, staging of resection of the giant AVM, and the judicious use of presurgical embolization or radiosurgery, or both, in an attempt to reduce the size of the arteriovenous shunt.

Evaluation

Angiography

Angiography remains the “gold standard” with respect to evaluation of AVMs. Because of the multiplicity of arterial feeders to these giant AVMs, it is important that a four-vessel angiogram be performed to document all of the arterial supply. Giant AVMs may have a portion of their blood supply from extracranial sources, so both external carotid arteries should be evaluated.⁴⁴ As with smaller AVMs, multiple views should be obtained to ensure that the neurosurgeon has a complete understanding of the origin of all the arterial feeders, the size and configuration of the AVM, and the number and direction of veins draining the AVM. A complete initial angiogram also allows better comparison with subsequent angiograms obtained during and after treatment. Angiography can also potentially document patients with a substantial amount of cerebrovascular steal as a result of the giant AVM. In these cases, normal cortical vessels may show more limited flow than other vessels at a distance from the AVM. In addition to standard two-dimensional angiography, the more recent development of three-dimensional angiography has improved the ability to identify the true size of the AVM (Fig. 389-1).⁴⁵

FIGURE 389-1 A 26-year-old woman underwent evaluation for seizures, which revealed a giant left parietal arteriovenous malformation (AVM). Three-dimensional cerebral angiography was performed to further characterize the AVM nidus (A-C). The portion of the AVM nidus filling from the posterior circulation is shown in red, whereas the portion of the AVM nidus filling from the anterior circulation is shown in green.

Post-treatment angiograms should be performed to ensure complete obliteration of the AVM, either soon after microsurgical resection of the final portion of the giant AVM or within several years after stereotactic radiosurgery if this modality is used as the final treatment within a staged approach to a giant AVM. It is critical to confirm complete treatment of an AVM, particularly giant AVMs, because leaving a residual AVM component is more problematic and reports suggest that partial treatment does not protect against future hemorrhage.^37,^38,⁴⁶^–⁴⁹

Angiography also plays an important role in the treatment of AVMs with stereotactic radiosurgery. Current radiosurgical systems rely on a fusion of angiography and magnetic resonance imaging (MRI) or computed tomography (CT) as a basis for planning treatment. In older radiosurgical systems, angiography is performed with a stereotactic base ring (or bite block) attached to the patient’s head and a fiducial cage mounted to the base ring. The fusion of angiography and MRI/CT allows improved targeting of the nidus while avoiding extraneous radiation doses to the draining veins or the surrounding cortical tissue. Newer image-guided radiosurgery is performed without a stereotactic ring, and in these cases, three-dimensional angiographic images can be directly fused to stereotactic CT and MRI during the treatment-planning process.⁴⁵

Magnetic Resonance Imaging

Although angiography remain the primary modality for evaluation of giant AVMs, pretreatment MRI provides additional information. MRI shows the relationship of the giant AVM to other intracranial structures, thereby affording the neurosurgeon a better understanding of the anatomy surrounding the AVM. The size and direction of large draining veins can often be noted, as can evidence of previous hemorrhage. MRI is also critical during the planning of stereotactic radiosurgery in conjunction with cerebral angiography. In select cases of giant AVMs with irregular shapes or deep components, intraoperative navigation with MRI-based guidance can be extremely useful. More recent developments in MRI technology have allowed the incorporation of three-dimensional imaging to assess both the AVM nidus itself ⁵⁰^–⁵³ and white matter tracts adjacent to the AVM.⁵⁴^–⁵⁶ Functional MRI has also been used to elucidate the relationship between an AVM and eloquent areas of the brain.⁵⁷

Xenon Computed Tomography

Xenon CT is rarely used in the evaluation of smaller AVMs, but for larger AVMs with significant surrounding cortical ischemia as a result of steal, this modality may be useful in determining the degree and distribution of hypoperfusion.⁵⁸ Impaired augmentation indicates failure of autoregulation and may identify patients at high risk for normal perfusion pressure breakthrough bleeding.

Treatment

Because of the relative infrequency of giant AVMs, which are thought to account for 10% of all AVMs,¹⁴ and the complexity of arterial feeders and venous drainage, treatment is individualized for each patient. It is rare for these giant AVMs to be treated successfully at a single sitting with one modality, and the best patient outcomes often involve staged treatment with two or more of the treatment modalities available.

Embolization

Because giant AVMs are difficult to treat with microsurgery alone and are too large to be optimal targets for stereotactic radiosurgery, embolization is generally the first course of treatment. Historically, this process consists of using either small polyvinyl alcohol particles ³¹ or cyanoacrylate glue⁵⁹^–⁶² in an attempt to occlude the feeding arteries. Over the past decade, n-butyl-2-cyanoacrylate (NBCA) has emerged as the main embolic agent of choice because its soft nature after occluding portions of the nidus does not interfere with later surgical resection of the AVM.⁶¹ Recently, ethylene vinyl alcohol copolymer (Onyx, Micro Therapnetics, Irvine, CA) has been studied as an embolic agent, with several clinical series documenting the efficacy of this agent.⁶³^–⁶⁷ The primary goal of embolization is to reduce volume and flow in the AVM to facilitate safer and more effective subsequent treatment with microsurgery or radiosurgery (or both). Embolization of deep feeders to the AVM or deep AVM components may help in later surgical resection. Occasionally, embolization alone is used for palliation of symptoms from giant AVMs with no intent of obliterating the entire lesion. Embolization is usually performed in several stages, often three or more, for giant AVMs.⁴⁴ Staged embolization allows the AVMs to adjust to changes in flow hemodynamics after each embolic treatment; attempts to embolize large portions of a giant AVM in a single stage are frequently associated with increased risk for hemorrhage. Giant AVMs can have a significant external carotid component, and embolization of these vessels often makes the craniotomy opening easier for the surgeon, as well as reduces blood supply to the AVM. Many giant AVMs have arterial supplies from both the anterior and posterior circulation and frequently from both hemispheres, and therefore multiple vessels need to be cannulated in an attempt to achieve optimal embolization. Care must be taken to avoid passing embolic glue or particles into normal cortical vessels to avoid the development of infarcts.

During embolization, patients with giant AVMs are monitored with electrophysiologic potentials, which provides several benefits.^39,⁴⁰ First, such monitoring is particularly useful in identifying when normal cortical vessels are inadvertently occluded. Second, electrophysiologic monitoring during embolization can also provide some insight to the neurosurgeon regarding whether the patient’s brain can tolerate periods of relative hypotension (which may be used later during surgery to reduce bleeding). This is particularly relevant when treating an AVM with “steal” or ischemic symptoms. Furthermore, when a particular vessel is in question, amobarbital sodium (Amytal) can be injected into the vessel before embolization to determine whether the vessel is supplying an area of eloquent cortex and hence would cause a neurological deficit if occluded.⁶⁸

Some institutions use intraoperative embolization extensively in treating giant AVMs.³¹ The advantages of this technique are that the risk of reflux into normal vessels is decreased and the surgeon has the opportunity to inject numerous distal vessels inaccessible to the neurointerventionalist in the angiography suite. Intraoperative embolization proceeds once the surgeon has performed the craniotomy and exposed the AVM. Injection of the embolic agent should be performed as close to the AVM nidus as possible to minimize reflux into normal vessels. After temporary occlusion of the proximal portion of the vessel, 27-gauge needles can be introduced and several cubic centimeters of NBCA injected. This process can be repeated for various feeding arteries until flow to the AVM is significantly reduced. After embolization, each feeding artery can be sacrificed with either a small clip or bipolar coagulation.

Stereotactic Radiosurgery

Stereotactic radiosurgery has established itself as successful treatment of certain intracranial AVMs, particularly small or moderate-sized AVMs located in critical brain regions. A number of clinical series using either heavy charged particles (protons and helium ions) or photons (Gamma Knife or linear accelerator) have demonstrated that AVMs less than 3 cm in diameter treated with 20 to 25 Gy equivalents (GyE) have a 3-year obliteration rate of 80% to 95% with a low complication rate (2.5% to 4.5% permanent neurological deficits, 2.5% to 4.5% transient deficits).^29,^37,^38,⁶⁹^–⁷⁷ However, various limitations of stereotactic focused radiosurgery have become apparent after analyzing the results in treating AVMs larger than 3 cm. These AVMs have a much lower obliteration rate, even after 3 years (33% to 58%), and a higher complication rate (20% to 30%) with treatment doses of 15 to 20 Gy.^29,^38,^70,^73,⁷⁵^–⁷⁹

The primary mechanism of AVM obliteration after radiosurgery involves hyperplasia of the vascular intima ⁸⁰ with progressive narrowing and ultimately occlusion. Such obliteration typically takes place over a 2- to 3-year period. There are three considerations when weighing surgery versus radiosurgery for the treatment of AVMs. First, AVMs larger than 4 cm in diameter have only a 33% to 50% rate of obliteration at 3 years after radiosurgery but a 20% to 30% complication rate with treatment doses of 15 to 20 Gy.^38,⁷⁷ The rate of obliteration is increased for larger AVMs when higher doses are used (25 to 45 Gy); however, the risk for radiation-induced complications increases significantly. Second, the risk for intracranial hemorrhage persists during the interval between treatment and complete obliteration.^38,^75,⁷⁷ Third, serial radiographic studies, including cerebral angiography, are necessary to confirm complete obliteration.

Despite these limitations, radiosurgery may be associated with less morbidity than surgical resection in patients with portions of giant AVMs in eloquent brain.^28,³⁰ Radiosurgery can be used as a preoperative adjunct to obliterate portions of giant AVMs and thus decrease the size of the remaining nidus for later surgical resection.²⁹ Some authors have recommended staged stereotactic radiosurgery when treating giant AVMs.⁸¹ In these cases, multiple radiosurgical treatments are delivered to different portions of the AVM at various intervals to avoid delivering treatment to a single large target. This theoretically reduces the risk for radiation necrosis.

Some patients with giant AVMs require more than one course of stereotactic radiosurgery, and this option has been used in selected patients.^29,⁸² The disadvantages of such an approach are the second latency period of 1 to 3 years before obliteration occurs, the possibility that a second radiosurgical treatment may still not obliterate the AVM, and the risk for radiation-induced injury, which may be higher with a second radiosurgical treatment.

Microsurgery

Generally, microsurgical resection of giant AVMs is planned after staged embolization or radiosurgery (or both) has significantly reduced the size of the AVM and the number of feeding arteries to the nidus. We routinely use corticosteroids and prophylactic antibiotics during resection of all AVMs, and patients are operated on under mild hypothermia (33°C) for neuroprotection. Patients also receive therapeutic levels of anticonvulsants, which are maintained at least during the acute postoperative period or longer if patients had seizures as part of their initial manifestation. Lumbar drainage or the administration of mannitol to achieve brain relaxation is individualized but generally used.

Patients are positioned in a manner to allow optimal exposure of the AVM while maintaining adequate jugular venous drainage. A supine position is preferred because it allows the optimal patient position for maintaining any femoral groin sheaths required for intraoperative angiography, which is difficult in the lateral position and impossible in the prone position. The head is elevated 15 degrees above the heart to improve venous outflow and reduce intraoperative bleeding. The head is placed in three-point head fixation for stabilization, and a radiolucent head frame is used if intraoperative angiography is planned.

The orientation of the incision in the scalp varies with the location and approach to each particular giant AVM, but it should be situated directly over the AVM whenever possible (Video 389-1). The bone flap should be made large enough to allow access to the entire AVM, even if staged resection is planned, because this would permit optimal exposure should any unexpected intraoperative bleeding occur. Hemostasis is achieved, dural tack-up sutures are placed, and the dura is opened in curvilinear fashion. Veins adherent to the dura can be taken down by bipolar coagulation and sharp dissection as long as they are not the primary draining veins. At this point, superficial giant AVMs are usually visualized on the cortical surface. For deeper AVMs that do not appear on the cortical surface, draining veins can be followed back to the malformation. Careful correlation between the pattern of vessels noted intraoperatively and previous angiograms usually allows determination of the major feeding arteries and draining veins.

Once identified, the AVM is resected in systematic fashion under guidance with the microscope, and systemic mean blood pressure is lowered to 60 to 70 mm Hg to minimize bleeding. Feeding arteries are located first and then individually coagulated and cut. The larger feeding vessels are clipped with Sundt micro-AVM or mini-aneurysm clips in addition to coagulation. It is important to proceed with treating one vessel at a time because hemorrhage from multiple sources can rapidly lead to significant bleeding and loss of control by the surgeon. Draining veins are often encountered before the feeding arteries are identified. It is imperative that venous drainage be preserved until all the arterial feeders are transected and the nidus is dissected out. Before transecting a vein, it is useful to first occlude it with a temporary aneurysm clip and observe the nidus. If the nidus begins to swell or bleed, the vein must be preserved until the final stages of resection. Intraoperative quantitative and directional ultrasound (Charbel Micro-flowprobe, Transonic Systems, Inc., Ithaca, NY) can also be used to differentiate arterialized veins from feeding arteries.

Dissection begins on the superficial border of the malformation, and circumferential dissection of feeding arteries is performed around the AVM, with care taken to stay within the gliotic plane immediately outside the AVM when working in noneloquent cortex. Gentle traction on the nidus with a moist cottonoid allows visualization of these feeding arteries. When dissecting adjacent to critical brain parenchyma, it is safer to dissect close to the AVM, even encroaching on the nidus, instead of risking injury to the surrounding brain. Once the superficial borders of the malformation are free, the AVM can be gently retracted so that the deep perforating arteries can be coagulated. Retractors should be adjusted frequently to allow optimal exposure for each particular surgical view. Meticulous hemostasis must be maintained throughout the resection. A self-irrigating or nonstick bipolar coagulation unit is extremely useful during the dissection. Fragile arteries resistant to coagulation can be occluded with Sundt micro-AVM clips. Judicious use of Surgicel (Johnson & Johnson, New Brunswick, NJ), Gelfoam (Pharmacia and Upjohn, Kalamazoo, MI), Avitene (Davol, Inc., Cranton, RI), and small pieces of bulk cotton can also be quite helpful in treating general oozing. Larger feeding arteries can be permanently occluded with Sundt mini-aneurysm clips (Codman and Shurtleff, Inc., Raynham, MA), but care must be taken to preserve any en passage vessels. These vessels are often difficult to identify at first, and care should be taken to follow each of these vessels and only cauterize them once the surgeon is sure that no normal cortex is being supplied by the vessel in question.

Deep ependymal feeding arteries are usually the last, but often the most problematic feeders to deal with. These vessels tend to be fragile, tear easily, and are often difficult to control with bipolar coagulation. Furthermore, they tend to retract into the surrounding brain tissue, which often requires the surgeon to dissect deeper than desirable to find the source of the hemorrhage. Patience on the part of the operating surgeon is required when occluding these vessels with bipolar coagulation or small Sundt microclips to halt bleeding.

The venous drainage of giant AVMs is generally both superficial and deep, but usually toward the midline. During AVM dissection, superficial draining veins can be gently retracted to increase exposure. When possible, draining veins should be sacrificed last, immediately before removal of the nidus; smaller draining veins may have to be sacrificed during resection of the AVM to facilitate removal. When working within the ventricular system, the ventricles should be protected against the accumulation of blood with cotton pads or bulk cotton. This will minimize the likelihood of hydrocephalus developing postoperatively. Once resection of the AVM is completed, the microscope should be used to inspect the resection bed for any signs of residual AVM, which is more likely to occur with giant AVMs that have irregular shapes than with smaller AVMs, and to achieve hemostasis. It is important to check for hemostasis at normotension or even mild hypertension. An intraoperative angiogram can be performed to ensure complete resection of the nidus, but because of the lower quality of these intraoperative images, a conventional angiogram in the radiology suite should also be performed in the postoperative period.

If the surgical procedure is staged because of the size of the AVM, the extent of surgical hemorrhage, or the risk for normal perfusion pressure breakthrough bleeding, the neurosurgeon needs to determine the optimal point at which to complete the initial stage. Giant AVMs frequently have irregular shapes, and resection of one or more lobes of these larger AVMs is often an ideal point to cease surgery. In other cases of AVMs extending down toward the basal ganglia and thalamus, resection of the superficial component of the AVM can be followed by a second stage involving resection of the deeper portion. In the event that the residual portion of the giant AVM after staged surgical resection would place the patient at significant neurological risk, this residual could potentially be treated by stereotactic radiosurgery. When staging surgical resection of AVMs, it is critical that the portion of the AVM exposed but not resected be carefully inspected to ensure hemostasis. If postoperative bleeding is noted, it is generally from the residual AVM.

Because giant AVMs generally involve several different lobes, a compartmental approach to resection may be required, even if the AVM nidus is to be resected in a single operation. For example, a giant AVM within the frontal and temporal lobes may be resected by removing the malformation first from the temporal compartment and, once this is completed, subsequently removing the AVM from the frontal lobe. Major sulci or fissures can assist the surgeon by serving as natural planes of dissection. Compartmentalizing the AVM resection allows the surgeon to operate on several discrete lobes of the AVM rather than on one giant malformation. Frequently, if staged surgeries are planned, surgical resection of one of the compartments/lobes of the AVM may be an ideal stopping point.

Another indication for surgical treatment of giant AVMs would involve resection of radiation necrosis. Radiation injury after stereotactic radiosurgery may result in significant mass effect and edema and require prolonged treatment with high doses of corticosteroids. We have observed several patients with steroid dependence as a result of radiation injury who were successfully tapered off corticosteroids after resecting areas of necrosis, as well as some patients who have shown substantial neurological improvement.⁸³

Before operative closure, meticulous hemostasis is obtained in the resection bed of the AVM, and a final inspection is performed to ensure that the entire malformation has been removed completely. Transient induced mild hypertension (90 to 100 mm Hg) is used to test hemostasis, and the resection bed is then lined with Surgicel. Frequently, a ventricular catheter is placed and connected to an external drainage bag if resection of the AVM has exposed the ventricle. The dura is closed in standard fashion with 4-0 nylon suture and the bone replaced to complete the craniotomy. A subgaleal drain is attached to light suction for 12 to 24 hours. The scalp incision is closed in two layers, the galeal layer is approximated with 3-0 Dexon suture, and the skin is closed with staples. Extubation should be performed in a smooth and deliberate fashion to avoid any elevations in intracranial pressure or venous pressure. During emergence from anesthesia, systemic blood pressure must be carefully monitored to avoid any hypertensive episodes. In cases in which there was significant normal perfusion pressure breakthrough, patients may be left intubated for several days to optimize blood pressure control.

In the intensive care unit, hypotension should be maintained for 24 to 48 hours to prevent rebleeding. Although we previously used prophylactic barbiturates postoperatively after resecting large or giant AVMs, we now use this technique only if uncontrollable bleeding is encountered. Coagulation studies should be performed and coagulation corrected if abnormal. Any changes in neurological findings should be evaluated with emergency CT. A postoperative angiogram is obtained in the first week after surgery unless an intraoperative angiogram was performed with adequate angiographic resolution to confirm complete AVM resection.

Multimodality Treatment

The complexity of giant AVMs often requires combinations of embolization, stereotactic radiosurgery, and microsurgery to achieve a complete cure. Our experience with large and complex AVMs has shown that such multimodality therapy can reduce patient morbidity and mortality.^27,^29,^30,⁸⁴ Embolization obviously reduces the volume of nidus requiring resection, but stereotactic radiosurgery delivered several years before surgical resection also produces a benefit. In some patients, partial AVM thrombosis significantly reduced the volume of residual AVM that required surgical resection. More importantly, at surgery the irradiated (but patent) AVMs were found to be much less vascular, even in nonembolized areas, than AVMs not previously irradiated. Radiosurgically treated AVM vessels were easier to occlude with bipolar coagulation, thus facilitating quicker and safer resection with less blood loss.²⁹ Although preoperative angiograms often demonstrate significant residual AVM after radiosurgery, observations at surgery suggest that the prior radiosurgery has obliterated the small-vessel component of the AVM not visible on the angiogram.⁸⁰ Our success in completely obliterating several previously irradiated AVMs with embolization alone also suggests that prior radiosurgery may thrombose a small-vessel component and leave larger arteriovenous fistulous portions of the AVM.^85,⁸⁶

Special Perioperative Equipment/Techniques

Intraoperative Monitoring

Electrophysiologic monitoring is an extremely valuable aid during procedures for midline or deep AVM resection and improves clinical results.^32,⁸⁷ Monitoring routinely consists of bilateral somatosensory evoked potentials and motor evoked potentials. Continuous monitoring of these sensory and motor pathways has allowed early detection of excessive retraction, manipulation of critical structures, excessive hypotension, or sacrifice of critical nonfeeding arteries, all of which are more likely to occur during resection of giant AVMs than during resection of smaller malformations. In addition, we have found brainstem auditory evoked potentials useful during the resection of posterior fossa AVMs.⁸⁷ Electrophysiologic monitoring has also proved useful in assisting in determination of the extent of AVM resection when staged procedures are planned. Frequently, changes in electrophysiologic monitoring result in cessation of further AVM resection. When these changes are detected early and surgery halted, potentials usually return to baseline and clinical worsening does not generally occur. Because giant AVMs are often located adjacent to motor and sensory cortex, intraoperative mapping has also proved useful in assessing the resectability of these lesions. Burchiel and colleagues used corticography and stimulation mapping to evaluate motor, sensory, and language cortex, with excellent results.⁸⁸

Frameless Image-Guided Navigation

Intraoperative navigation helps localize portions of deep AVMs not seen directly at the ventricular or pial surface. Image-guided navigation such as with the Medtronic Stealth Station (Medtronic, Minneapolis, MN) has high reliability and typically maintains a precision of a few millimeters during the procedure. Other intraoperative navigation systems include the Radionics Omnisight Excel System (Radionics, Inc., Burlington, MA) and the Brainlab VectorVision System (Brainlab, Inc., Westchester, IL). These intraoperative navigation systems have allowed better planning for exposure of deeper AVMs and have also helped confirm complete resection of all components of giant AVMs that may have irregular configurations.

Mild Hypothermia

Mild brain hypothermia can be used for cerebral protection. Core body and brain temperature is decreased to 33°C by applying a cooling blanket or using an intravascular catheter cooling system (Innercool Therapies, San Diego, CA).⁸⁹ This degree of mild brain hypothermia has been shown to provide excellent protection against experimental ischemic and traumatic cerebral injury,⁹⁰ and we have used it at Stanford for more than 2600 intracranial procedures with good results. Under the operative conditions of AVM resection, this hypothermic technique is safe, feasible, and economical with good clinical outcomes overall.

Intraoperative Angiography

Intraoperative angiograms have been possible with the advent of high-resolution portable angiography and allow the surgeon to determine the completeness of AVM resection.⁹¹ If residual AVM is present, the surgeon has an opportunity to complete the resection before closure of the wound. At least two studies have shown that patients are not protected with partial resection of AVMs,^4,⁹² so complete resection remains the goal for all AVMs. In two other studies, 10% to 18% of surgical procedures for resection of AVMs were altered by the results of intraoperative angiography.^93,⁹⁴ We routinely use intraoperative angiography for resection of most giant AVMs to document the completeness of resection and sometimes to assess the extent of residual AVM for deliberate staged surgery.

Intraoperative Doppler Blood Flow Measurements and Ultrasound

Intraoperative ultrasound for measuring blood flow can have several uses. First, ultrasound can determine whether flow through veins is arterialized. Such knowledge allows the surgeon to establish whether the nidus still has a significant arterial source and thus whether the vein in question can safely be transected. Second, directional and quantitative ultrasound can help distinguish feeding arteries from arterialized draining veins, as well as establish flow rates through individual feeding arteries. Nornes and Grip were able to estimate total AVM flow in 9 of 16 patients (range, 150 to >900 mL/min; average, 490 mL/min).¹² They were also able to make pressure recordings from feeding arteries at their entrance to the AVM and showed that this pressure was well below systemic arterial blood pressure in all cases (ranging from 40 to 77 mm Hg; average, 56 mm Hg). For deep AVMs, ultrasound can be used to locate the malformation, which can facilitate the planning of cortical incisions, identification of the vessels involved, and determination of the surgical approach.⁹⁵

Surgical Outcome

There are few published series exclusively consisting of giant AVMs because most authors have included these vascular malformations in larger series of general vascular malformations. Anson and Spetzler reported a series of 32 giant AVMs (all were Spetzler-Martin grade V lesions).³¹ After combined therapy, 15 patients were clinically improved, 7 were unchanged, and 10 had worsening deficits, although 8 of these 10 deficits were either transient or mild.³¹ Seven patients required two surgical stages and 4 patients required three surgical stages to complete the AVM resection. Three of the 4 patients undergoing three operations also required presurgical embolization (three courses each) to reduce AVM size.

Heros and coauthors reported 21 patients with giant AVMs in a series of 153 AVM patients.⁹⁶ Early good or excellent results were achieved in 61% of grade IV patients and 29% of grade V patients. Patients improved with longer follow-up; a 12% morbidity and mortality rate for grade IV giant AVMs and a 38% rate for grade V malformations were demonstrated.

Fifteen patients with AVMs larger than 5 cm were reported in a series of 90 AVM patients by Hernesniemi and Keranen.⁹⁷ Of these patients, 5 had excellent outcomes, 6 had moderate disabilities, 1 had a severe disability, 1 died, and 2 were lost to follow-up. These authors recommended staged resection and several days of induced systemic hypotension to prevent breakthrough bleeding.

We have treated 53 patients (20 males and 33 females) at Stanford with giant AVMs larger than 6 cm.²⁷ Twenty of these patients (38%) were seen initially with hemorrhage, 8 (15%) with headache, 18 (34%) with seizures, and 7 (13%) with progressive neurological deficits. One patient had a Spetzler-Martin grade III AVM, 9 had Spetzler-Martin grade IV AVMs, and 43 had Spetzler-Martin grade V AVMs. The mean AVM size was 6.8 cm (range, 6 to 15 cm). AVM venous drainage was superficial (n = 7), deep (n = 20), or both (n = 26). At initial evaluation, 31 patients (58%) were graded as being in excellent neurological condition, 17 were graded good (32%), and 5 were graded poor (9%). Treatment included surgery (n = 27; 51%), embolization (n = 52; 98%), or radiosurgery alone or combined with surgery or embolization (n = 47; 89%). Most patients received multimodality treatment consisting of embolization followed by surgery (n = 5), embolization followed by radiosurgery (n = 23), or embolization, radiosurgery, and surgery (n = 23) (Figs. 389-2 to 389-5). Nineteen patients (36%) were completely cured of their giant AVMs, 90% obliteration was achieved in 4 patients (8%), less than 90% obliteration was achieved in 29 patients (55%) who had residual AVMs even after multimodality therapy, and 1 patient was lost to follow-up. Of the 33 patients who either completed treatment or were alive more than 3 years after undergoing their most recent radiosurgery, 19 (58%) were cured of their AVMs. The long-term treatment-related morbidity rate was 15%. The clinical results after a mean follow-up of 37 months were 27 excellent (51%), 15 good (28%), 3 poor (6%), and 8 dead (15%).

FIGURE 389-2 A 30-year-old man suffered headaches, intractable seizures, and a left hemiparesis as a result of a previous hemorrhage from a 7 × 4.5 × 4.5-cm right parietal arteriovenous malformation (AVM) extending into the basal ganglia and thalamus. Initial magnetic resonance imaging showed the AVM on an axial view (A). Initial angiography showed the AVM filling from the right internal carotid injection on anteroposterior (B) and lateral (C) views. The patient underwent heavy-particle radiosurgery at a dose of 17.5 GyE to a volume of 88,000 mm³. Two years after radiosurgery, there was no change in the angiographic appearance of the AVM, so the patient underwent two courses of embolization, with postembolization right carotid anteroposterior (D) and lateral (E) angiographic views showing partial reduction in AVM volume. The patient underwent microsurgical resection of the residual AVM, with a final right carotid angiogram showing complete obliteration on anteroposterior (F) and lateral (G) views. The patient’s headaches resolved, his seizures were significantly improved, and he had no new neurological deficits.

FIGURE 389-3 A 33-year-old man had three previous hemorrhages from a giant right frontotemporal arteriovenous malformation (AVM), as seen on pretreatment axial (A) and coronal (B) magnetic resonance images. Initial angiography, anteroposterior (C) and lateral (D) views, showed the AVM filling from a right carotid injection. The patient underwent two courses of embolization with a resultant 50% reduction in volume of the AVM. The patient was then treated with heavy-particle stereotactic radiosurgery at a dose of 20 GyE to a volume of 72,000 mm³. The patient underwent a third course of embolization, with further reduction in AVM volume, as seen on anteroposterior (E) and lateral (F) right carotid views. The residual AVM was then microsurgically resected, and postoperative right carotid angiography showed complete obliteration of the AVM on anteroposterior (G) and lateral (H) views. The patient had some mild left-sided hemiparesis postoperatively, but this resolved completely over the next 6 months.

FIGURE 389-4 A 34-year-old man had a 2- to 3-year history of headaches that were precipitated with bending forward. Initial evaluation included magnetic resonance imaging, which showed a giant arteriovenous malformation (AVM) in the right mesial temporal lobe on axial (A) and coronal (B) images. Initial angiography showed the AVM filling on anteroposterior (C) and lateral (D) carotid injections. The patient underwent three embolizations, which resulted in a 40% reduction in AVM volume. This was followed by 15-GyE stereotactic radiosurgery to a volume of 47,500 mm³. Three years after radiosurgery, there was still partial filling of the AVM, and a fourth course of embolization was performed, which further reduced the size of the AVM, as seen on anteroposterior (E) and lateral (F) carotid views. The residual AVM was resected with microsurgery, and postsurgical angiography confirmed obliteration of the AVM, as seen on anteroposterior (G) and lateral (H) carotid angiograms. Clinically, the patient remained neurologically intact with the exception of new left upper quadrantanopia.

FIGURE 389-5 A 25-year-old man was evaluated for headaches, a bruit, episodes of visual distortion, and memory difficulties. Magnetic resonance imaging revealed the presence of a giant left parietal AVM, as seen on an axial image (A). Initial left carotid angiography showed the AVM filling on anteroposterior (B) and lateral (C) views. He underwent stereotactic radiosurgery with 18 Gy as his initial treatment. Three years after radiosurgery, there was no significant reduction in AVM volume, so two courses of embolization were administered, which resulted in a 40% reduction in AVM volume, as seen on anteroposterior (D) and lateral (E) left carotid angiograms. The patient was then taken to the operating room, where intraoperative electrophysiologic mapping showed that the AVM was posterior to the somatosensory cortex. Total resection was achieved, as seen on anteroposterior (F) and lateral (G) left carotid angiograms. The patient had an initial mild right hemiparesis and hemisensory deficit that resolved completely over the next 6 months.

Complications

Hemorrhage

The most devastating complication is postoperative hemorrhage (Fig. 389-6), which fortunately is extremely rare. It can be due to either inadequate hemostasis, failure to completely resect the AVM, or normal perfusion pressure breakthrough. Postoperative hemorrhage can be minimized by careful inspection and hemostasis of the resection bed after removal of the AVM and by a short period of induced hypertension after resection but before closure to check for breakthrough bleeding. Intraoperative angiography and image-guided navigational systems can also aid in confirming complete AVM resection. After surgery, hypotension is maintained in the intensive care unit for 1 to 2 days to permit adjustment of the cerebral vasculature to the new hemodynamics. Normal perfusion pressure breakthrough bleeding can be minimized by staging surgical procedures to allow a gradual change in cortical vasculature flow dynamics after each procedure, followed by several days of deliberate hypotension after final resection of the AVM. Hemorrhage can also occur after embolization of AVMs and occasionally result in the need for emergency craniotomy to remove blood clots.⁹⁸ This risk is reduced by staging embolization procedures and maintaining a 12-hour period of relative hypotension after the procedure.

FIGURE 389-6 A 26-year-old woman with a giant left temporal-occipital arteriovenous malformation (AVM) underwent proton beam radiosurgery. However, she continued to deteriorate with medically intractable seizures, progressive memory impairment, and right homonymous hemianopia. Four years later her AVM was unchanged angiographically from the pre-radiosurgical appearance, as seen on axial (A) and sagittal (B) magnetic resonance images and on a lateral left internal carotid artery angiogram (C). The patient underwent four embolization procedures, with a postembolization lateral left carotid angiogram (D) showing a significant reduction in AVM volume. The patient was the scheduled for repeated heavy-particle radiosurgery but suffered a fatal hemorrhage, shown on computed tomography (E), 1 week after her last embolization.

Venous Thrombosis

Venous thrombosis may occur in the early postoperative period or occasionally after embolization. A sudden reduction of flow in the enlarged draining veins predisposes to this phenomenon, which may cause parenchymal swelling, hemorrhage, and severe neurological deficits. We avoid fluid restriction postoperatively in an attempt to minimize this problem.

Hydrocephalus

Postoperative hydrocephalus is a known complication in patients with significant intraventricular blood. Any intraventricular clot secondary to previous hemorrhage should be removed before resection of the AVM. In addition, meticulous hemostasis should be maintained throughout the procedure to minimize any acute ventricular blood. If significant intraventricular blood is present, a ventriculostomy can be placed before closure. Long-term hydrocephalus is treated by placement of a ventriculoperitoneal shunt.

Radiosurgical Complications

Adverse sequelae from radiation are broadly classified according to their time of appearance with respect to treatment.^99,¹⁰⁰ Complications from radiosurgery can be similarly categorized. Acute reactions are defined as occurring during, immediately after, or within the first several days of therapy and primarily consist of nausea and emesis. These symptoms occur in 10% to 16% of patients within 6 hours of treatment.¹⁰¹ Preventive measures include pretreatment with antiemetics and steroids.¹⁰¹ Late reactions occur more than 3 months after therapy and are usually associated with some degree of permanent neurological injury. Because of the large tissue volume of giant AVMs treated by stereotactic radiosurgery, the potential for adverse sequelae is greater than for smaller targets.

Although seizures can occur after stereotactic radiosurgery, they are also associated with the underlying pathology in many patients. Consequently, it is not always clear whether a seizure is directly related to treatment. Kjellberg and coworkers reported a small increase in acute seizure risk in AVM patients treated with proton radiosurgery.⁴⁷ Similarly, it has been our experience at Stanford that there is a slightly increased risk for seizures within the first 48 hours after radiosurgery, especially when treating large AVMs in eloquent cortex. Post-treatment seizures often correlate with subtherapeutic levels of anticonvulsants in patients who are receiving these agents. We regularly augment standard anticonvulsant doses on the day of radiosurgery to achieve a “high therapeutic” level in patients at risk for post-treatment seizures and have found that this practice minimizes these adverse events during the immediate post-treatment period.

Symptomatic radiation necrosis and edema remain the most debilitating of the late complications caused by stereotactic radiosurgery. Histologic changes in the affected brain consist of neuronal death, gliosis, and both endothelial proliferation and hyalinization.^80,¹⁰² The reported incidence of radiation necrosis varies between 2.3% and 20%,^38,¹⁰³^–¹⁰⁵ and it generally occurs 6 to 9 months after treatment, with larger AVM volumes likely to result in increased risk for injury. Current treatment of the edema that accompanies radiation necrosis is corticosteroids. The time course of symptoms and the need for steroids are typically quite protracted, with up to 1 year or longer needed before resolution. In severe cases of necrosis, surgical resection can ameliorate the mass effect and significantly improve the clinical status of some patients.