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Cerebral Arteriovenous Malformation Diagnosis and Management Kaiz Asif, MD1

John Leschke, MD1

Marc A. Lazzaro, MD1,2

1 Department of Neurology, Medical College of Wisconsin and

Froedtert Hospital, Milwaukee, Wisconsin 2 Department of Neurosurgery, Medical College of Wisconsin and Froedtert Hospital, Milwaukee, Wisconsin

Address for correspondence Marc A. Lazzaro, MD, Departments of Neurology and Neurosurgery, Division of Neurointervention, Medical College of Wisconsin/Froedtert Hospital, Milwaukee, WI (e-mail: [email protected]).

Abstract Keywords

► arteriovenous malformation ► radiosurgery ► embolization ► hemorrhagic stroke

Arteriovenous malformations of the brain can carry considerable morbidity and mortality in the setting of rupture. The complex angioarchitecture and hemodynamic alteration requires careful consideration in diagnostic and management approaches. In this review, the authors define the pathophysiology, outline diagnostic methods, and highlight current management approaches.

An arteriovenous malformation (AVM) consists of a complex tangled web of single or multiple arteries linked to single or multiple draining veins through an abnormal intervening network of vessels.1–3 Although AVMs are rare, the associated high morbidity and mortality underscores the need for careful consideration in diagnosis and management of these vascular abnormalities. Specifically, an understanding of the pathophysiology, hemodynamic disturbance, imaging features, and treatment options is necessary.

Biology, Pathophysiology, and Hemodynamics Fundamentally, AVMs are congenital vascular lesions that arise from a disruption of normal vascular morphogenesis during fetal development.4 Arteriovenous malformations are deficient in an intervening capillary bed, but the precise mechanism of pathogenesis remains unknown. Vascular morphogenesis proceeds in two stages embryologically. Vasculogenesis occurs initially as endothelial cells arise from angioblasts to form a primary vascular plexus. Angiogenesis occurs thereafter with remodeling and organization of the primary vascular plexus mediated by a complex array of protein signaling pathways.5–9

Issue Theme Advanced Cerebrovascular Disease Management; Guest Editor, Jason Mackey, MD, MS

Clinical and laboratory observations offer a collection of theories describing this pathological progression. Some suggest that AVMs represent a persistence of the congenital vascular plexus with failure of the necessary venous/arterial remodeling.10 The fact that almost half of AVMs are located in arterial borderzone territories can be explained by the theory that AVMs may arise from persistent artery to artery connections during the lissencephalic state in the primitive cortex.11 In the normal state, these connections regress as the cortical architecture develops and the gyri are formed, ultimately giving rise to the leptomeningeal system; hence, AVMs are thought to arise within or after the formation of arterial border zones.12 Others have suggested that AVMs are dynamic in nature and a product of a proliferative capillaropathy.13 Arteriovenous malformations might even represent fistulized cerebral venous angiomas.14–16 Arteriovenous malformations can be located anywhere throughout the cerebral vascular system. They can be restricted to the dura or choroid plexus and can vary widely in size, such that some require microscopy for visualization, but others can involve an entire hemisphere. The distal arterial branches are more commonly involved, predominantly involving the distribution of the middle cerebral artery and the hemispheric convexities.17 Generally, AVMs manifest as solitary lesions; multiple lesions are relatively rare. Multiple

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DOI http://dx.doi.org/ 10.1055/s-0033-1364212. ISSN 0271-8235.

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Semin Neurol 2013;33:468–475.

lesions rarely occur spontaneously and are most commonly observed in syndromic settings with cutaneous or extracranial vascular anomalies18 such as Rendu-Osler-Weber disease and Wyburn-Mason syndrome. Brain AVMs are often pyramid-shaped such that the base is adjacent the cortex and the vertex projects internally toward the ventricles. Arteriovenous malformations are further differentiated anatomically based on the involvement of brain parenchyma. A compact nidus is a malformed capillary bed that is tightly organized such that normal brain parenchyma is displaced. A diffuse nidus is loosely organized with sparse, abnormal AV channels such that normal brain parenchyma persists.19 The appearance of an AVM on catheter angiography can highlight these characteristics (►Fig. 1). The velocity of blood flow is considerably higher through AVMs than through normal brain parenchyma. As a result of

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the abnormal hemodynamic condition, feeding arteries and draining veins become progressively dilated and tortuous. Normal vascular structures undergo a series of secondary changes. Feeding arteries may be one or numerous and experience high flow arteriovenous shunting due to absence of capillary networks. Because of constant intraluminal stress there is abnormal dilation, degenerative changes with aberrant elastic lamina, variability of medial thickness in the vessel wall, and architectural disarray.2,20–22 High flow may result in new pathology such as saccular aneurysm formation. These aneurysms can be located at the level of the circle of Willis, the feeding arteries, or within the nidus.23–26 Additionally, high flow can produce progressive stenosis and eventual occlusion of feeding arteries.27 Draining veins can be single or multiple, deep or cortical, and are also exposed to increased intraluminal stress. Direct shunting of blood at arterial pressure causes dilatation, thickening, and tortuosity in the involved veins. High flow may also produce localized stenosis, frequently at the level where the veins cross the dura to reach the sinus,28,29 and secondary venous aneurysmal dilatation.30

Epidemiology Establishing a true prevalence of AVM is difficult because of the rarity of the disease and the presence of asymptomatic patients; prevalences are likely underestimates. Large postmortem studies are still needed. Only a few hospital-based postmortem studies are available, reporting a prevalence between 400 and 600 per 100,000.22,31,32 Much of what is known about incidence is from population-based studies. Over a 10-year-period in the Netherlands Antilles, the annual incidence of symptomatic AVMs was 1.1 per 100,000 per year.33 In another study, the incidence of symptomatic AVMs was 1.84 per 100,000 per year.34 The New York Islands AVM Study, a prospective population-based incidence and casecontrol study, found an annual AVM detection rate of 1.34 per 100,000 person-years. Arteriovenous malformations are found incidentally on 0.05% of brain magnetic resonance imaging (MRI) screens.35 There are very few familial cases. Arteriovenous malformations are more commonly identified in younger individuals. Detection in utero or in infancy is rare,36–38 and the diagnosis is most commonly made between 30 and 40 years of age. Both sexes are affected in nearly equal proportions.33,39

Clinical Presentation

Fig. 1 A high-frame-rate catheter angiogram captures several distinct components of an arteriovenous malformation including feeding artery supply (A, arrows), nidus (B, circle), and venous outflow (C, arrow), which must be separated by fractions of a second due to the high flow.

The clinical presentation of these lesions can vary and include signs of intracranial hemorrhage (focal deficits, nausea, vomiting, etc.), seizures, and headaches. Intracranial hemorrhage is a common cause of symptomatic presentation,40 and often is the presenting feature in the second through fourth decades of life.41 Seizures at presentation have been reported to occur in  30% of patients. Headaches have been reported in 14% of patients.39 The clinical presentation may be affected by the size and location of the lesion. Seminars in Neurology

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Cerebral Arteriovenous Malformation Diagnosis and Management

Cerebral Arteriovenous Malformation Diagnosis and Management

Diagnosis The diagnosis of an AVM is usually made via noninvasive imaging (computed tomography [CT] or MRI), but the therapeutically relevant anatomical and functional information often requires catheter cerebral angiography.

Computed Tomography and Magnetic Resonance Imaging Because the most common clinical manifestations are not specific for AVM, the first imaging modality is usually a noncontrast CT. Certain factors would warrant further evaluation for an AVM in a patient who presents with spontaneous intracranial hemorrhage. Young patients with lobar parenchymal hematoma or otherwise unexplained intraventricular hemorrhage or subarachnoid hemorrhage require additional imaging. Findings of curvilinear or speckled calcifications and serpiginous hyperdense structures can represent draining veins, components of the nidus, or dilated arterial feeders.39,42–44 Confirmation of the diagnosis and evaluation of the vascular and parenchymal details is necessary. Although a CT angiogram could provide better vascular details, an MRI with an MRA might allow better visualization of parenchymal changes. Magnetic resonance imaging can allow evaluation of eloquence of the involved brain, perinidal or

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intranidal gliosis, parenchymal atrophy with focal dilatation of the ventricular system, presence of an old hematoma (hemosiderin on gradient echo [GRE] sequences), hydrocephalus in cases of prior hemorrhage, and ventricular system compression by enlarged draining veins.45,46 Multimodal imaging is often necessary to confirm a diagnosis of AVM as demonstrated in ►Fig. 2.

Digital Subtraction Angiography Digital subtraction angiography (DSA) is considered the gold standard for the evaluation of cerebral AVMs. Although noninvasive imaging provides structural understanding of an AVM, pretherapeutic planning often necessitates DSA to allow excellent spatial as well as temporal resolution, which is required for assessing the nidus size, assessing feeding arterial and draining venous stenosis, and evaluating for flow-related arterial and intranidal aneurysms and draining venous aneurysms.47 Moreover, planning of endovascular embolization can be performed using superselective microcatheter angiography, which allows targeting of specific feeding arterial branches and further angioarchitecture characterization. The addition of threedimensional (3D) rotational angiography to DSA aids in understanding complex 3D characteristics and allows superior determination of the radiation target if radiosurgery is planned.48,49

Fig. 2 (A) Diagnostic imaging for evaluation of suspected right frontal arteriovenous malformation (AVM) shows hemorrhage on a noncontrast head computed tomography (CT) scan. (B) Magnetic resonance (MRI) brain T2 sequence image demonstrates flow voids adjacent to the hemorrhage consistent with an AVM nidus. (C) Catheter angiography defines the angioarchitecture of the lesion. (D–G) Sequential frames in a lateral projection angiogram of the right frontal AVM show abnormal artery architecture arising from the right pericallosal artery with early cortical vein filling and rapid outflow through the superior sagittal sinus. Seminars in Neurology

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Functional Imaging Assessment of the eloquence of brain tissue involved with AVMs with blood-oxygen-level dependent (BOLD) functional MRI could help in avoiding damage to the eloquent brain areas before embolization, surgical resection, or radiosurgery. In this way BOLD can help shorten the surgical time and achieve smaller craniotomies.50,51 One of the major limitations of the task-based functional MRI for AVMs and vascular tumors is the phenomenon of neurovascular uncoupling, which occurs when dysplastic vessels do not demonstrate appropriate BOLD activation of the normal functioning neurons.52

Natural History For unruptured AVMs, the rate of rupture has not been welldefined, though reports include annual risks of up to 2 to 4% in patients with an initial nonhemorrhagic presentation and a widely varying lifetime risk of hemorrhage estimated to be 17 to 90%.53 High-risk features for rupture including nidal aneurysms and angiographic flow characteristics are often considered, but consensus on the importance of these features has not been established. For ruptured AVMs, the risk of rehemorrhage after first hemorrhagic presentation has been reported as 6 to 18% in the first year, after which it is  2% per year for the next 20 years.54

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tem. It added three more variables: Age (< 20 years: 1 point, 20–40 years: 2 points, > 40 years: 3 points), prior history of rupture (ruptured: 0 points, not ruptured: 1 point), degree of diffuseness (compact: 1 point, diffuse: 0 point) with grades ranging from I to V. They analyzed a consecutive surgical series of 300 patients to compare the predictive accuracy using the Spetzler-Martin scale and the supplementary scale and found the scale had high predictive accuracy and stratified surgical risk more evenly. The supplementary grade can be considered separately, with supplementary grades I to III having an acceptably low risk of AVM resection. The supplementary scale can also be added to the Spetzler-Martin grade, with combined grades 1 to 6 having an acceptably low surgical morbidity. In cases of mismatched Spetzler-Martin and supplementary grades, the supplementary grading system can potentially play a role in altering clinical decisions, though more data on the application of this grading system is required.57 A separate classification system for grading in endovascular therapy has also been proposed. This classification system includes AVM size, number of feeding arteries, and pial versus perforating feeding arteries. Low-grade AVMs that were considered suitable for endovascular therapy were small, had fewer than two feeding arteries, and were not supplied by perforators, whereas high-grade AVMs that were large (> 4 cm), had more than four feeding arteries, and were supplied by perforators were not suitable for endovascular therapy.58

Classification Systems The Spetzler-Martin classification is used to grade AVMs based on their degree of surgical difficulty and the risk of surgical morbidity and mortality. The grade is based on the size of the AVM (< 3 cm: 1 point, 3–6 cm: 2 points, > 6 cm: 3 points), venous drainage (superficial only: 0 points, deep: 1 point) and eloquence of adjacent brain (eloquent: 0 points, noneloquent: 1 point), with grades ranging from I to V. Arteriovenous malformations too complex for resection, including brainstem and holohemispheric AVMs, were given grade VI. Low-grade AVMs (grades I and II) have relatively low surgical morbidity rates and are commonly treated surgically, while high-grade AVMs (grades IV and V) have relatively high surgical morbidity rates and are commonly managed conservatively. Grade III AVMs are somewhat more challenging and are the most heterogeneous of the five grades.55 Grade III AVMs have been further divided into four different combinations: small-deep-eloquent (S1V1E1), medium-deep (S2V1E0), medium-eloquent (S2V0E1), and large (S3V0E0). Based on a consecutive series of 76 grade III AVMs, Lawton et al found that neurologic outcomes varied according to the subtype of grade III AVM. They found that small-deep-eloquent (S1V1E1) AVMs had surgical risks similar to low-grade AVMs, but that medium-eloquent (S2V0E1) AVMs had surgical risks similar to high-grade AVMs. Medium-deep (S2V1E0) had intermediate surgical risks.56 Lawton and colleagues subsequently introduced a supplementary grading system to the Spetzler-Martin grading sys-

Management Due to the lack of robust natural-history data and the limited understanding of features thought to be associated with a high risk of hemorrhage, the management of AVMs remains complex. The choice between procedural management and observation with medical management and radiologic surveillance is not always clear-cut. The high morbidity and mortality associated with ruptured AVMs often warrants a procedural approach, with the goal of AVM eradication. Treatment modalities include endovascular embolization, surgical resection, and radiosurgical intervention. Randomized studies comparing treatment approaches are lacking. The specifics of each case are considered and a tailored teambased approach is often required.

Observation Unruptured AVMs with a nonhemorrhagic presentation are often considered for observation, which includes medical management and surveillance imaging. The ARUBA (A Randomized Trial of Unruptured Brain Arteriovenous Malformations) Trial compared medical management with invasive treatment in patients with unruptured AVMs. The ARUBA Trial halted enrollment after a preplanned interim data safety monitoring board review identified a higher event rate in the intervention group compared with medical management.59 Although early event rates were higher in the intervention arm, patients will be followed to determine whether the difference in stroke and death in the two arms changes Seminars in Neurology

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Cerebral Arteriovenous Malformation Diagnosis and Management

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over time. Medical management for symptomatic unruptured AVMs includes anticonvulsants in patients with seizures, medications for headache, and optimization of blood pressure control. Surveillance imaging is performed to evaluate for changes in AVM size and morphology, though the optimal surveillance strategy is unclear. Surveillance is commonly performed on a yearly or biennial basis.

Endovascular Treatment With the advent of improved endovascular technology, sophisticated microcatheter designs, and embolic materials with desirable properties, endovascular embolization of AVMs has become increasingly common. The goal of endovascular therapy is to achieve complete cure in small AVMs with favorable characteristics for an endovascular approach, or for partial targeted embolization in conjunction with surgical resection or in combination with stereotactic radiotherapy. Embolization materials include liquid embolics, such as n-butyl cyanoacrylate and ethylene vinyl alcohol copolymer (Onyx), and platinum embolic coils. Feasibility of endovascular treatment depends on the angioarchitecture of the AVM, with small size and a single feeding artery being favorable features for complete curative embolization. Although it is technically demanding to catheterize a large number of small, minimally dilated feeding arteries, advanced microcatheter designs and flowguided ultrathin microcatheters have allowed delivery beyond tortuous anatomy (►Fig. 3). Complete cure of the AVM has been reported in up to 20% of cases.60

Fig. 3 Lateral projection angiogram images demonstrate a large left parieto-occipital arteriovenous malformation (A) with near-complete obliteration following liquid embolization (B).

Partial targeted embolization is preferred for larger AVMs. For presurgical embolization, the goal is to reduce the size of the AVM and to embolize deep feeding vessels, which would be difficult to access surgically. When combined with

Fig. 4 Magnetic resonance brain T2 sequence images (MRIs) show a large left basal ganglia arteriovenous malformation (AVM) with an enlarged left internal cerebral vein at diagnosis (A). Follow-up MRI at 1 year (B) and 2 years (C) after radiosurgery show significant progressive reduction in the AVM nidus. Lateral projection catheter angiogram images for radiosurgery targeting at diagnosis demonstrate arteriovenous shunting through the left basal ganglia AVM (D–G). Seminars in Neurology

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Approach

Benefits

Limitations

Endovascular embolization

Catheter delivery of

Minimally invasive Real-time angiography

Obliteration rate can be lower depending on characteristics Risk of ischemic complications during treatment

Surgical resection

Microsurgical excision

High rates of complete obliteration

Invasive due to craniotomy

Radiotherapy

Focal radiation is administered to the lesion

Noninvasive

1–3 year latency for obliteration Parenchymal radiation injury Limited to smaller lesions

• Liquid embolics (n-butyl cyanoacrylate glue, Onyx) • Coils

radiosurgery, the target of embolization is often the periphery of the AVM to reduce the size and therefore the total radiation dose required.61,62 Clinically significant complications have been reported to occur in  6.5% cases.63

Surgical Resection Microsurgical excision involves creating a craniotomy centered over the nidus followed by careful devascularization of the AVM by occluding the arterial feeders. Circumferential separation of the AVM from the adjacent parenchyma is performed and the draining veins are then divided.64 Intraoperative electrophysiologic monitoring is often performed using electroencephalography, somatosensory evoked potentials, and in the case of posterior fossa AVMs, brainstem auditory evoked potentials.65 Postoperative angiography is performed to confirm complete excision. The risk of microsurgical approach is assessed using the Spetzler-Martin grading system with higher grades associated with greater surgical morbidity and mortality.55,66 A metaanalysis reviewing several series from 1990 to 2000 showed a mean global mortality of 3.3% and mean postoperative global morbidity of 8.6%.67

thalamus/basal ganglia/brainstem]).72 The proportion of AVMs obliterated without a new neurologic deficit was greater than 90% for a score less than 1 and less than 40% for a score more than 2.73 Various approaches for treatment of AVMs continue to develop and often involve complementary interventions in complex lesions to afford a greater success rate (►Table 1).

Conclusions Arteriovenous malformations are rare developmental vascular lesions that often present in younger individuals with intracranial hemorrhage, seizure, or headaches. Rates of intracranial hemorrhage are low, but high morbidity and mortality necessitate a careful consideration of management risks and benefits. Current treatment approaches include medical management, endovascular liquid embolization, focal radiosurgery, and surgical resection.

References 1 The Arteriovenous Malformation Study Group. Arteriovenous

Stereotactic Radiotherapy Stereotactic radiosurgery aims at achieving progressive obliteration of an AVM using intense high-dose radiation produced by a radiation source (including gamma knife, linear accelerators, or proton-beam) and delivered accurately and precisely using a navigation system (►Fig. 4). Obliteration of the AVM occurs via endothelial damage and thickening of intimal layer followed by thrombosis and necrosis of AVM vessels,68 a process which takes  2 to 3 years with a median of 2 0 months required to obtain subtotal (> 95%) obliteration.69,70 The nidus geometry and neighboring at-risk structures are determined using thin-slice MRI and CT, which are used to formulate radiosurgery treatment plans. Successful obliteration with radiosurgery is dependent on various factors, including nidus volume, nidus density, radiation dose, and location.71 The modified radiosurgery-based grading scale incorporates some of these factors and is calculated as follows: (0.1  volume in mL) þ (0.02  age in years) þ (0.5  location [0 for hemispheric/intraventricular/callosal/cerebellar AVMs and 1 for AVMs involving the

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Table 1 Treatment approaches for cerebral arteriovenous malformations

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Seminars in Neurology

Vol. 33

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Cerebral Arteriovenous Malformation Diagnosis and Management

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Cerebral arteriovenous malformation diagnosis and management.

Arteriovenous malformations of the brain can carry considerable morbidity and mortality in the setting of rupture. The complex angioarchitecture and h...
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