54 Spetzler–Martin Grade III Arteriovenous Malformations
Abstract
Arteriovenous malformations (AVMs) are rupture-prone tangles of dysplastic blood vessels with direct arteriovenous shunting that may lead to neurological deficits through hemorrhage, mass effect, and/or alterations in blood flow. Morbidity of surgical intervention is commonly estimated by the Spetzler–Martin grading scheme. For lesions with an intermediate grade, such as Spetzler–Martin III AVMs, optimal treatment remains controversial and often involves a multidisciplinary approach. A nuanced approach and further substratification of patients is required to assist clinical decision making and to maximize likelihood of a good clinical outcome. This chapter addresses several controversies in treating Spetzler–Martin III AVMs—including whether treatment is indicated, patient selection for multimodal therapy, supplementary and additional classification schemes to guide treatment allocation, and technical nuances for both microsurgical and endovascular treatments.
Introduction
Brain arteriovenous malformations (AVMs) are a rupture-prone tangle of dilated and dysplastic blood vessels in which arterial blood is directly shunted into the venous circulation without an intervening capillary bed. In the majority of patients—a reported range of 42 to 72%—intracranial hemorrhage is the first clinical manifestation. AVMs account for roughly 2% of all hemorrhage strokes. In the absence of overt hemorrhage, microhemorrhage, mass effect, and/or alterations in local hemodynamic factors with associated ischemic steal phenomenon give rise to clinical symptoms—including headache, seizure, and/or focal neurological deficits. Early detection and treatment of brain AVMs irrespective of treatment modality are thus of paramount importance.
Major controversies in decision making addressed in this chapter include:
Whether or not treatment is indicated.
Patient selection for multimodal therapy.
Addition of supplementary classification schemes and further substratification to guide clinical decision making in Spetzler–Martin III AVMs.
Nuances for the microsurgical and endovascular management of AVMs.
Whether to Treat
The decision to treat a brain AVM requires a calculated balance between the risks of hemorrhage, neurological decline, and treatment. The annual rate of hemorrhage for unruptured AVMs is approximately 1 to 4%. After initial hemorrhage, the rate of rehemorrhage increases to approximately 6 to 10% for the first year and then declines to that of an unruptured AVM for each subsequent year. A simplified approach to estimate one′s lifetime risk of hemorrhage is illustrated by the formula: Rupture risk = 105–patient age in years. However, these estimates are crude, and the risk for hemorrhage from individual AVMs may be much higher ( 1 , 2 in algorithm ). For example, a study from the Columbia AVM databank has suggested higher additive risk with additional factors (range 0.9–34%)—including deep brain location, exclusively deep venous drain, and presentation with hemorrhage. Other studies have shown that the relative risk of AVM hemorrhage increases with intranidal aneurysms or feeding artery aneurysms by a factor of 2.28- and 1.8-fold higher, respectively ( 1 , 2 in algorithm ). Despite these nuances, what is clear is that AVM hemorrhage is infrequently a clinically benign event with rates of morbidity and mortality estimated to be between 25 and 50% and 10 and 20%, respectively.
A number of potential of treatment modalities are in the neurosurgeon′s armamentarium—including microsurgical resection, endovascular embolization, stereotactic radiosurgery, and medical management. Effective treatment of an AVM often requires a multidisciplinary approach between neurosurgeons, interventional neuroradiologists, and radiation oncologists to utilize multiple treatment modalities. With publication of the Randomised trial of Unruptured Brain AVMs (ARUBA), some have argued against invasive management, and decisions to treat AVMs must be balanced against treatment-associated morbidity and mortality. In our opinion, given the significant neurological morbidity of an untreated AVM, definitive treatment when safe should be attempted. Several clinical decision-making algorithms have been developed to aide with patient selection, and the approach utilized at the University of California San Francisco will be described in ensuing subsections.
Classification
The Spetzler–Martin grading scale is a long-standing clinical scoring system that provides a preliminary assessment of surgical risks and guides treatment decision making in brain AVMs. Its relative simplicity has led it to become the most widely utilized clinical classification schemes of brain AVMs. However, a noted limitation of the Spetzler–Martin grading system is that of its predictive value in intermediate grade III AVMs—a heterogenous clinical entity comprising multiple distinct subtypes with different treatment ramifications. Treatment recommendations in the Spetzler–Martin grade III AVMs require an individualized approach with consideration of additional factors and often multimodality treatment planning.
Anatomical Considerations
The Spetzler–Martin grade III AVMs are the most heterogenous of the five Spetzler–Martin grades that may yield distinct anatomical subtypes (▶ Fig. 54.1 ). As with other AVMs, in order to correctly identify the subtype, careful preoperative evaluation of both the pattern of venous drainage and functional importance of the surrounding brain parenchyma is essential. Venous drainage is deemed superficial if veins drain into cortical veins, the venous sinuses around the convexity, or, in the instance of posterior fossa lesions, the straight and/or transverse sinuses (▶ Fig. 54.1a, c ). Deep venous drainage, on the other hand, implies drainage into the vein of Galen or its associated venous structures—including the internal cerebral vein, basal vein of Rosenthal, and the precentral cerebellar vein. Lesions are considered eloquent if located within the sensorimotor cortices (▶ Fig. 54.1a, b ), cortical regions devoted to language, visual cortex, hypothalamus, thalamus, internal capsule, brainstem, cerebellar peduncle, or deep cerebellar nuclei.
For the purposes of discussion, those with a nidus of less than 3 cm will be considered small, whereas those with a nidus of 3 to 6 and greater than 6 cm will be referred to as mid-sized and large, respectively. Under the conventional Spetzler–Martin grading scheme, four distinct subtypes are possible. These include a small nidus size with deep venous drainage in eloquent locations (S1V1E1), a medium nidus size with deep venous drainage in noneloquent locations (S2V1E0), a medium nidus size with superficial venous drainage in eloquent locations (S2V0E1), and a large nidus size with superficial venous drainage in noneloquent locations (S3V0E0). The surgical risks for each subcategory are discussed in ensuing subsections, and we propose an alternative classification in which S1V1E1, S2V1E0, S2V0E1, and S3V0E0 will be subsequently referred to as grade III–, grade III, grade III+, and grade III*, respectively, as this better approximates their risk profile.
In addition to these characteristics, attention should be paid to whether hemorrhage is present, the morphology of the nidus, and the presence of deep artery perforators—which are thin, fragile, and difficult to occlude. Unlike aneurysm surgery, AVMs often require transgression of otherwise functional brain tissue. The presence of a hematoma helps separate AVMs from adjacent brain, minimizes transgression of normal brain, and may create avenues of access that are otherwise unavailable. Hemorrhage and resulting thrombosis may also decrease some of the arterial supply to the AVM helping with intraoperative blood loss. A compact nidus also helps with the ease of resection with distinct boundaries and dissection planes that minimize transgression of brain parenchyma. A diffuse nidus, on the other hand, is a loosely woven tangle of vessels with interdigitating brain parenchyma. The inclusion of normal brain into dissection planes in these scenarios is unavoidable, and may represent an important component of surgical morbidity.
Workup
Clinical Evaluation
AVMs mostly come to clinical attention as a result of intracerebral hemorrhage—reported range of 42 to 72% of cases. Presenting symptoms include headaches, seizures, focal neurological symptoms, or, in the case of severe hemorrhage, alterations in the level of arousal. A complete and thorough neurological examination with neuroimaging, when indicated, is appropriate to discern the etiology of the patient′s symptoms.
Imaging
Noncontrast computed tomography (CT) scan with concurrent or subsequent CT angiography are effective first imaging modalities to detect acute hemorrhage with an underlying vascular lesion. This should be followed, when available, with digital subtraction angiography as this remains the gold standard to evaluate an AVM′s angioarchitecture. Magnetic resonance imaging (MRI), including functional MRI or diffusion tensor imaging when indicated, and MR angiography provide detailed information regarding the relationship of the AVM with the surrounding brain structures. Specialized navigational sequences help facilitate frameless stereotaxic navigation when the AVM is not readily visible on the cortical service. Digital subtraction angiography is essential in confirming the diagnosis, analyzing anatomical details for surgery, and for accurate grading.
Differential Diagnosis
The differential diagnosis for intracerebral hemorrhage is expansive and beyond the scope of the present chapter. Vascular lesions that may closely mimic the appearance of an AVM on vascular imaging include dural arteriovenous fistulas and highly vascular tumors, for example, hemangioblastomas and high-grade gliomas.
Treatment
Choice of Treatment and the Influence of Intracerebral Hematoma
The judicious selection of patients to avoid surgical complications and poor neurological outcomes with microsurgical resection of brain AVMs is essential. Conventionally, this has been accomplished through Spetzler–Martin grading. Low-grade AVMs (grades I and II) are associated with low rates of surgical morbidity (0–5%) and are frequently treated surgically. High-grade AVMs (grades IV–V) have comparatively higher morbidity (12–38%) with surgical resection, and therefore are managed conservatively or with other treatment modalities, for example, radio-surgery. For grade III AVMs, we advocate further subcategorization as risks are not equivalent for all subtypes—as described in the Anatomical Considerations subsection. For grade III lesions, surgical resection is generally safe. Those deemed grade III lesions require individualized treatment planning, whereas grade III+ lesions have risks that exceed traditional Spetzler–Martin grade III lesions and are better suited for conservative management and/or other treatment modalities.
In addition to the Spetzler–Martin grading, other factors should be considered when predicting surgical risk. As previously described, presentation with hemorrhage generally favors surgical resection and facilitates surgical access. In other settings, it may necessitate immediate operative intervention due to alleviate refractory intracranial hypertension. In recognition of the value of additional clinical information, our group has devised and validated a supplementary classification scheme—which is designed to complement, but not replace the Spetzler–Martin grading. Points are assigned for patient age (< 20 years, 1 point; 20–40 years, 2 point; > 40 years, 3 points), hemorrhage at presentation (0 points, hemorrhage; 1 point, no hemorrhage), and compactness of the nidus (0 points, compact; 1 point, diffuse; 2, 3, 4 in algorithm ). As with the Spetzler–Martin grading, these points are summed to provide a supplementary AVM grade. Our works have demonstrated that this has higher predictive accuracy than the Spetzler–Martin system and leads to a more even stratification of risk. We advocate a tiered approach in which the Spetzler–Martin grade provides an initial risk estimate (summarized in ▶ Fig. 54.1 ), but then application of the supplementary grading system further refines patient selection for AVM surgery. Supplementary grades ≤ 3 have low risk of morbidity with surgical resection or, if combined with the Spetzler–Martin grade, AVMs with a combined score of ≤ 6 have an acceptably low risk for surgical morbidity. In many instances, application of the supplementary scale confirms initial Spetzler–Martin risk assessment. However, in grade III AVMs with intermediate surgical risk or in cases in which Spetzler–Martin and supplementary grades are mismatched, application of the supplementary scale may alter treatment decisions.
Despite our surgical focus, optimal management rarely involves one treatment modality and a complementary approach among specialists—especially with Spetzler–Martin grade III AVMs—is required. Application of our tiered approach determines whether AVMs are suitable for surgery. Once eligibility of microsurgical resection is determined, AVMs eligible for microsurgical resection should then be evaluated for embolization. If embolization with low associated risk is possible, the patients should undergo dual modality therapy. If embolization proves too risky or would unnecessarily delay care—such as in settings with a hematoma and elevated intracranial pressures—microsurgical resection without embolization should proceed ( 3, 5, 6 in algorithm ). Patients that are poor surgical candidates, for example, a combined Spetzler–Martin and supplementary grade greater than 6, should be assessed as to whether they are a candidate for radiosurgery with the intention of reducing AVM volume and making the AVM more favorable for surgical resection ( 4, 7, 8 in algorithm ). AVMs with a nidus ≤ 3 cm in diameter are best treated with single-session stereotactic radiosurgery ( 7, 9 in algorithm ). A nidus that exceeds 3 cm, however, is generally not amenable to conventional stereotactic radiosurgery (SRS) as the marginal dose would exceed that which is safe ( 7, 10 in algorithm ). These lesions are best treated with volume-stage radiosurgery and should be reassessed throughout and at the end of a 3-year latency period to monitor for level of obliteration. Those which are incompletely obliterated should be re-evaluated for resection with preoperative embolization.
Conservative Management
Lesions not amenable to therapy or select unruptured AVMs as demonstrated in the ARUBA trial may be managed medically—namely, symptomatic treatment of neurological symptoms, for example, antiepileptic medications, and aggressive optimization of vascular risk factors, for example, hypertension, diabetes, and smoking cessation. Neuroimaging surveillance is also an important component. Patients must be routinely evaluated for the development of associated aneurysms on feeding arteries, within the nidus or in the circle of Willis. Aneurysms ≥7 mm in diameter and/or which appear dysplastic should be considered for treatment.
Open Cerebrovascular Management: Operative Nuances
Each AVM is a unique admixture of feeding arteries, draining veins, nidal vessels, and therefore has a distinct set of technical obstacles. Each craniotomy should be tailored to the AVM anatomy. AVMs may be classified based on brain location and the cortical surface from which it is based—this helps dictate the most appropriate craniotomy and approach to perform (▶ Table 54.1 ). In general, craniotomies should be large to maximize visualization, permit wide subarachnoid dissection, and allow free manipulation of surgical instruments. When planning the approach, a delicate balance must be achieved by achieving maximal visualization to the AVM surface and feeding vessels while minimizing transgression of normal brain and eloquent regions. To facilitate this, care must be emphasized with preoperative planning and patient positioning. With the head optimally positioned, gravity retraction in combination with subarachnoid dissection and release of cerebrospinal fluid can open anatomical plans for surgical access without violating the pial surface. Dural structures—such as the falx cerebri or tentorium—may also be utilized to prevent the sag of other neural structures from obstructing the surgical view (▶ Fig. 54.2 ).
In our surgical experience with Spetzler–Martin grade III lesions, the most common type was a small nidus with deep venous drainage in an eloquent location (grade III lesions). These require a surgical approach that capitalizes on subarachnoid dissection down cerebral fissures to deep locations to make these lesions readily accessible without significant retraction. For medial supratentorial lesions—including the corpus callosum, thalamus, and intraventricular lesions—this may involve the interhemispheric fissure. For sylvian or insular lesions, a transsylvian approach may be utilized (▶ Fig. 54.2 ). In the posterior fossa, multiple subarachnoid corridors may be accessed through established approaches—including supracerebellar infratentorial, retrosigmoid, and far lateral approaches. When AVMs are not accessible through anatomic subarachnoid corridors, a transcortical approach is unavoidable, but should utilize hematomas and/or encephalomalacia whenever possible. Transcortical trajectories should be carefully monitored with frameless stereotactic guidance (▶ Figs. 54.3 and 54.4 ).
Once reaching the AVM, the first priority is to identify and preserve draining veins until the end of resection (▶ Figs. 54.2 – 54.4 ). Arterialization of venous structures complicates this, and any vessel greater than 4 mm should be treated as a vein until proven otherwise. The course of the vessel to and from the AVM, close observation of muscular striations—which are more prominent in arteries—and temporary test occlusions help one discern venous from arterial structures. Secondary veins should be handled with similar care, and only bipolared in proportion to a reduction in arterial inflow. In general, these are safe to be sacrificed when they become dark in coloration and the AVM tolerates temporary occlusion of the vessel destined for sacrifice. Pial dissection in AVM surgery is unavoidable and should be initiated along arterial fonts—sites rich in feeding arteries. Initial resection should focus on arterial feeders. They should be occluded and sacrificed as close to their point of contact with the nidus of the AVM as possible. This is best accomplished by walking the coagulating tips of the bipolar electrocautery in proximal to distal direction along a 3- to 7-mm portion of the feeding artery. Microclips may be applied, if the vessel resists occlusion with electrocautery. Complete circumdissection of the pia and brain tissue surrounding an AVM is needed to advance the resection, and every artery feeder encountered should be interrupted (▶ Figs. 54.2 – 54.4 ). Judicious use of retractors may help increase visualization of deep surfaces, but should be applied cautiously to avoid kinking or tearing of fragile draining veins. Attention should be paid to preoperative functional imaging, for example, functional MRI or diffusion tensor imaging, as well as intra-operative frameless navigation when the eloquence of adjacent brain parenchyma is of concern.
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