BRAIN ARTERIOVENOUS MALFORMATIONS BRAIN ARTERIOVENOUS MALFORMATIONS

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Advances in Radiosurgery for Arteriovenous Malformations of the Brain Benjamin A. Rubin, MD Andrew Brunswick, MD Howard Riina, MD Douglas Kondziolka, MD NYU Langone Medical Center, New York, New York Correspondence: Douglas Kondziolka, MD, NYU Langone Medical Center, 530 First Ave, Ste 8R, New York, NY 10016. E-mail: [email protected] Received, June 1, 2013. Accepted, October 11, 2013. Copyright © 2014 by the Congress of Neurological Surgeons

Arteriovenous malformations of the brain are a considerable source of morbidity and mortality for patients who harbor them. Although our understanding of this disease has improved, it remains in evolution. Advances in our ability to treat these malformations and the modes by which we address them have also improved substantially. However, the variety of patient clinical and disease scenarios often leads us into challenging and complex management algorithms as we balance the risks of treatment against the natural history of the disease. The goal of this article is to provide a focused review of the natural history of cerebral arteriovenous malformations, to examine the role of stereotactic radiosurgery, to discuss the role of endovascular therapy as it relates to stereotactic radiosurgery, and to look toward future advances. KEY WORDS: Arteriovenous fistula, Arteriovenous malformation, Embolization, Endovascular, Gamma Knife, Radiosurgery Neurosurgery 74:S50–S59, 2014

DOI: 10.1227/NEU.0000000000000219

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erebral arteriovenous malformations (AVMs) are vascular lesions that can be a source of substantial neurological morbidity and mortality for patients who harbor them. The current treatment paradigms for cerebral AVMs involve very different strategies that can include surgical resection, endovascular embolization, stereotactic radiosurgery (SRS) alone or in combination, and in some cases simple observation.1,2 This multimodal approach requires the expertise of a multidisciplinary team to determine which modality may be optimal for any given patient. Dural arteriovenous fistulas (DAVFs) represent a specific subtype of vascular malformation for which similar treatment modalities may be used. Again, due because of the complexity of these lesions, a multidisciplinary approach is required to optimize treatment and outcomes.1 Many AVMs are not amenable to surgical resection because of the unacceptable morbidity related to their deep or critical brain location. For these lesions, in particular, recent advances in both endovascular techniques and SRS have ABBREVIATIONS: ARE, adverse radiation effect; ARUBA, A Randomized Trial of Unruptured Brain Arteriovenous Malformations; AVF, arteriovenous fistula; AVM, arteriovenous malformation; DAVF, dural arteriovenous fistula; MMP, matrix metalloproteinase; SRS, stereotactic radiosurgery

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allowed new strategies of treatment that provide unique therapeutic opportunities, potentially with enhanced efficacy and improved outcomes. In this article, we review the natural history of cerebral AVMs, explore the role of SRS and its technical nuances, examine ways in which these various modalities can be used in conjunction, and look toward future advances in the field of SRS for AVMs and DAVFs.

NATURAL HISTORY OF AVMS The natural history of AVMs has not been precisely elucidated because the exact incidence and prevalence of asymptomatic AVMs are not known.2 Furthermore, the natural history of asymptomatic and unruptured AVMs may differ somewhat because ruptured AVMs appear to have a higher hemorrhage risk than previously unruptured AVMs.2,3 The most common presenting symptom of an AVM is intracerebral hemorrhage, but other common symptomatology may include headache, seizures, or progressive neurological deficits. Typically, younger patients, those ,40 years of age, are affected, and there does not appear to be any male-female predilection.4-10 The annual risk of hemorrhage for all intracerebral AVMs is between 2% and 4% per year.3,5,6,9-14 For AVMs that have ruptured, the annual risk of rerupture increases in the first

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year after initial hemorrhage to between 6% and 8%, but after the first year, the risk reapproaches that of the prehemorrhagic risk profile.9,15 The morbidity related to hemorrhage is variable, but some reports find it to be as high as 80%. Mortality rates associated with these hemorrhages are not as high but are still significant, ranging from 10% to 30%.10,11,16 Mortality is highly dependent on brain location, with posterior fossa AVMs having a higher risk of hemorrhage-associated morbidity and mortality. Stratification of AVMs based on the unique characteristics of the lesion can also change the risk of rupture and, in some cases, increase it substantially. Locational characteristics such as close proximity or involvement of the ventricular system or involvement within the basal ganglia or other deep structures tend to increase the risk of hemorrhage and morbidity related to hemorrhage. If the lesion harbors perinidal, intranidal, or flowrelated aneurysms, then the risk of hemorrhage also increases. Additionally, the pattern of blood flow through the lesion or the presence of deep venous drainage patterns or of a single draining vein can also confer higher risk to a lesion.11,17-23 With so many variables interacting to directly affect the risk of hemorrhage, it is important to factor a comprehensive view when selecting the most appropriate treatment plan, including observation alone.

ARUBA TRIAL DESIGN, RESULTS, AND IMPLICATIONS Recently, the National Institutes of Health stopped accrual in A Randomized Trial of Unruptured Brain Arteriovenous Malformations (ARUBA), which compared observation with treatment for unruptured AVMs. The study began in 2007 and by 2010 had randomized 124 patients.24 The goal was to determine outcomes at a minimum of 5 years between those patients undergoing treatment (surgery, endovascular, SRS, or combination) and those in which observation alone was selected. The primary outcomes to be studied were death, stroke, and functional status, and the initial goal was to randomize 400 patients. There was early criticism of the study out of concern that the initial 5-year follow-up was insufficient for the natural history hemorrhage rate to exceed the complication rate associated with any given intervention. In response, the investigators increased the follow-up to a 10-year period. The study endured other criticism as well, including failure to truly randomize on the basis of AVM subtypes and the lack of a standardized therapeutic plan.24 By the time the study was halted in early 2013, it was determined that medical management of unruptured AVMs was superior to any given intervention.25 The Data Safety Monitoring Board had determined that the threshold for safety and efficacy had been met. The trial had enrolled 223 of its planned 400 patients. The data, released at the XXII European Stroke Conference in May 2013, showed that 109 patients had been randomized to conservative treatment and 114 others had undergone intervention for their AVMs. Mean follow-up was 33 months. The primary outcome of death or stroke was seen in

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11 patients (10%) in the conservative group and 39 patients (29%) in the interventional group. The interventional group also suffered worse functional outcomes.26 According to these data, it is clear that early intervention (without specifying technique) carries a higher risk of complication compared with conservative management as defined in this study. However, the long-term results remain unknown. The ARUBA investigators plan to continue to follow up this group to determine whether the differences persist.26 It can be speculated that on a longer time scale the complications of conservative management alone may approach, and perhaps even exceed, the short-term complications of treatment. Thus, the best management choice for incidentally identified AVMs remains to be determined but should be highly individualized. Thus, it is important to continue to investigate and study various treatment modalities to improve our understanding and our ability to deliver safe and efficacious treatment.

SRS FOR AVMS The potential for substantial morbidity and mortality associated with these lesions and their respective treatments requires the careful selection of an appropriate treatment plan that maximizes outcomes and minimizes risks to the patient. There exists a vast collective experience that shows that SRS, as a minimally invasive technique, can produce excellent results with a modest risk profile. It has therefore become an increasingly attractive option to both patients and physicians.27-34 The primary risks to a patient after SRS, as opposed to microsurgical resection, are 2-fold. First, after SRS, there is a latency period to obliteration during which the lesion remains at risk for hemorrhage. Second, as with any form of local intervention, adjacent structures can be affected, leading to neurological morbidity. The latter are referred to as adverse radiation effects (AREs).35 The latency period to obliteration after SRS, in which the lesion maintains a similar or slightly lower preradiation risk of hemorrhage, can be up to 4 years. Complete obliteration rates vary between 50% and 90%, depending on AVM volume.10,27,29,36-39 Once complete obliteration is confirmed by imaging or angiography, the lesion can be considered cured with ,1% risk of subsequent hemorrhage.37 Successful obliteration after SRS depends directly on the amount of radiation delivered and accurate identification of the AVM shunt, but the morbidity of SRS is a function of the radiation dose and the total volume treated. Therefore, a balance must be struck between maintaining treatment efficacy while minimizing AREs. Because the final target volume is a function of the intrinsic properties of the lesion and cannot be modified, dose selection in radiosurgery is a critical step in planning.37,40-50 Several early animal models and subsequent human clinical experience in AVM SRS generated both dose-response and dosecomplication curves. The goal was to achieve ,3% permanent risk of adjacent brain injury. The lower doses needed to achieve

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this risk inevitably lead to lower obliteration rates, especially in larger-volume AVMs. Compensation strategies have been developed to combat this limitation, including dividing the lesion into several defined volumes and staging SRS over several sessions (Figure 1).51-55 Optimum dose delivery for complete obliteration can be achieved by carefully balancing the dose-response and the dose-complication curves when creating the SRS dose plan56,57 (Figure 1). Dose planning involves a team of specialists, including a neurosurgeon, a radiation oncologist, and a medical physicist. To optimize the dose and improve efficacy while minimizing AREs, stereotactic and volumetric axial plane imaging in conjunction with digital subtraction angiography is needed to obtain a complete conformal dose plan. Some practitioners have used magnetic resonance imaging as the single imaging modality or magnetic resonance imaging in conjunction with computed tomography angiography. However, magnetic resonance imaging with digital subtraction angiography remains the gold standard by which a true conformal dose plan can be formulated to optimize safety and to increase the chance of obliteration.58-62 To achieve this aim, it is crucial to target the arteriovenous shunt. Doses at the margin of an AVM typically vary from 16 to 25 Gy in a single procedure, and obliteration rates tend to improve when the marginal dose equals or exceeds 17 Gy. The margin dose should be anywhere from 50% to 80% of the delivered dose at the center of the target to protect adjacent parenchyma and to achieve satisfactory obliteration rates.49,57 Achieving optimal dose planning helps to minimize AREs. Postradiosurgery inflammatory changes with blood-brain barrier effects and radiation necrosis can present clinical challenges, particularly when they occur in critical brain locations.63 AVMs adjacent to critical structures are at the highest risk for symptomatic effects because the clinical manifestations of ARE are related to the functionality of the affected region. The present pharmacological strategy for ARE treatment usually first involves high-dose glucocorticoids, often tapered slowly over 1 to 2 months. Another well-tolerated option is the combination of pentoxifylline and vitamin E, which can be used over an extended time frame. Rarely, anticoagulation, barbiturates, hypothermia, or hyperbaric oxygen therapy is used.64 There are some early data that treatment with bevacizumab may improve functional outcomes and radiographic features of radiation necrosis in patients treated with SRS for brain metastasis.63,65 One case report details its use for an AVM.66 Regardless of treatment strategy, clinicians must remain vigilant of the symptoms related to the acute, early, or even late manifestations of AREs when treating patients with SRS.

EMBOLIZATION AND SRS Embolization is commonly used as an adjunct to SRS for the treatment of AVMs. Traditionally, embolization has been used before SRS. The theoretic goal is to reduce the size of the AVM nidus, making it a manageable target for SRS. In many cases,

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embolization has been shown to reduce AVMs that are too large for SRS to sizes in which SRS can be used.29,67-84 The clear goal is volume reduction rather than flow reduction. Reduction of flow may have some benefit to enhance vessel obliteration, but this is not well characterized. Significant controversy exists regarding both the benefit of embolization and the timing with relation to SRS. Some have argued that embolization decreases the risk of hemorrhage during the latency period before AVM obliteration, although no definitive proof of this exists to date.12,68,72,75,83-92 Others have concluded that embolization has no effect on hemorrhage risk or may even increase the hemorrhage risk beyond the natural history by suddenly altering blood flow dynamics in vulnerable vessels.74,84,93-96 More troubling is the fact that embolization before SRS may lead to worse overall outcomes for patients who receive SRS. Multiple case series have shown that SRS obliteration rates for patients who receive prior embolization are significantly lower than for those who do not receive embolization.38,74,85,89,94-99 Multiple theories exist to explain the mechanism behind this finding. Some have asserted that the radiopaque embolic agents may act as a radioprotectant, scattering ionizing radiation and leading to decreased absorption by nidal vessels and therefore decreased obliteration.85,100 We find this theory to be unconvincing, and there are data to show that these embolic agents have a negligible influence on dose attenuation.101 Some have also postulated that eliminating the principal AVM feeders while leaving small feeders open can lead to growth of the unoccluded portions of the AVM via neoangiogenesis induced by ischemia.67,72,74,80 Partial embolization may divide the AVM into a series of discrete clusters, which further inhibits efforts at radiosurgery planning.38,46,71,75,84,85,89,92 Furthermore, irregularly shaped targets require greater radiation doses to surrounding normal parenchyma, which may explain the association of embolization with delayed cyst formation98 and brain edema67 after SRS. Perhaps the most likely reason for increased treatment failures with preoperative embolization is that radiosurgery planning becomes significantly more difficult. These agents alter the 3-dimensional appearance of the nidus and obscure nidal margins, leading to improper targeting and thus poor obliteration rates. Onyx (Covidien, Irvine CA) in particular causes significant magnetic resonance imaging artifact, obscuring AVM visualization102 (Figure 2). Furthermore, a recent study of pathological changes after embolization found evidence of recanalization in 18% of AVMs.103 If thrombosed segments are excluded from the radiosurgery plan, this will presumably contribute to additional treatment failures. If nearly 1 in 5 AVMs embolized ultimately fail, the theoretical benefit of embolization in shrinking AVMs to facilitate SRS is obviated. It has been shown that embolization leads to complete AVM obliteration in approximately 2% to 16% of AVMs.68 In light of these findings, one must question whether this obliteration is durable enough to forego SRS. Special consideration must be given to AVMs that are associated with intranidal or extranidal aneurysms or arteriovenous fistulas

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FIGURE 1. Volume-staged Gamma Knife radiosurgery plan (16 Gy to the 50% isodose line) for a 12-year-old girl with a thalamic arteriovenous malformation (AVM). Axial (A), coronal (B), and sagittal (C) T1-weighted contrast-enhanced magnetic resonance images (MRIs) showing an anatomic component of the first (blue line) and the second (yellow) volumestaged stereotactic radiosurgery. Angiograms showing the thalamic AVM at the time of Gamma Knife radiosurgery (D and E). Axial T1-weighted contrast-enhanced MRI showing total obliteration (F). Angiogram showing total obliteration 38 months after the second volume-staged radiosurgery (G).

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FIGURE 2. Post-Onyx embolization dose planning and targeting before Gamma Knife radiosurgery. Magnetic resonance imaging demonstrates artifact from the embolization obscuring visualization of the nidus. This can lead to less accurate identification of the arteriovenous malformation nidus and potentially lower long-term obliteration rates.

(AVFs). AVMs containing high-flow AVFs have been shown to be more resistant to radiosurgery87,104-107 and to have a higher incidence of perioperative hemorrhage,108-110 so strong consideration should be given to embolization in these lesions before SRS. AVMs may have associated aneurysms in 3% to 17% of cases.37,111-113 These aneurysms constitute an additional significant risk of hemorrhage, with annual bleeding risk varying from 7% to 11%.21,37,114 The 5-year risk of hemorrhage after SRS may be as much as 10 times greater in those patients harboring aneurysms, so aggressive surgical or endovascular treatment of these lesions is also indicated (Figure 3).

RADIOSURGERY FIRST, THEN EMBOLIZATION Because of the evidence showing poorer obliteration rates in AVMs receiving embolization before SRS, one option may be to consider embolization after SRS. Early reduction in flow after SRS may increase obliteration rates and decrease the length of the interval period in which the patient is at risk of hemorrhage. We and other groups are exploring this concept. Postradiosurgery endovascular treatment of associated aneurysms and AVFs may further decrease the hemorrhage risk. Another potential role for embolization may be the injection of radiosensitizing agents into

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the vascular endothelium just before, during, or immediately after SRS. For example, injection of selected endothelial growth factors may stimulate endothelial cell proliferation and lead to more rapid luminal occlusion.102

POTENTIAL PHARMACOLOGICAL INTERVENTIONS Basic science research has demonstrated that AVMs possess inherent pathological characteristics that may predispose them to hemorrhage. There is evidence of inflammatory cell involvement,115 which may lead to release of matrix metalloproteinases (MMPs), which can cause pathological vessel remodeling.116 MMP-9 is a proteolytic enzyme that degrades extracellular matrix proteins, cell surface proteins, and other substances surrounding the cell. This can cause destabilization, which can lead to weakening of the vessel wall.117,118 AVMs have been shown to possess increased levels of MMP-9 activity compared with normal tissue.119 Tetracyclines have been shown to inhibit the expression of MMPs. Hashimoto et al118 performed a pilot study in which AVM tissue was exposed to doxycycline ex vivo, followed by an in vivo administration to patients with AVMs for 1 week before resection. In both cases, the pathological specimens examined

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FIGURE 3. Post-Gamma Knife management of a coexisting intranidal aneurysm. Axial T1 postcontrast (A) and axial T2 (B) Gamma Knife magnetic resonance imaging showing left frontal arteriovenous malformation. Cerebral angiography for Gamma Knife planning with lateral (C) and anteroposterior (D) views demonstrating evidence of a coexisting aneurysm. Patient had Gamma Knife followed by partial embolization. Follow up digital subtraction angiography 4.5 months after Onyx embolization in lateral (E) and anteroposterior (F) views without evidence of residual aneurysm.

showed decreased levels of MMPs compared with controls. Frenzel et al120 completed a phase I trial of doxycycline and minocycline for patients with brain AVMs. This study concluded that it was safe to proceed to a phase II trial, although, to date, none has been completed. A separate pharmacological adjunct to radiosurgery may be the use of 21-aminosteroids to provide protection against brain radiation injury. These compounds block the release of free arachidonic acid from injured cell membranes, which may prevent a cascade leading to chronic radiation vasculopathy. The 21-aminosteroids exert their effects on endothelial cell membranes, inhibiting free-radical– induced lipid peroxidation, which can cause cell injury and lead to vasculopathy.121 Importantly, these compounds do not seem to inhibit necrosis, so the effects of radiosurgery on the lesion itself should not be blunted. In an animal model, rats treated with the 21-aminosteroid U74389G were shown to develop less vasculopathy and edema compared with controls; there was no difference in gliosis between the 2 groups.122

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RADIOSURGERY FOR DAVFS DAVFs constitute a heterogeneous group of lesions that may be classified as traumatic, associated with aneurysmal rupture, iatrogenic, spontaneous, congenital, and idiopathic. Taken as a whole, the annual rupture risk of a DAVF is approximately 1.5%,123 although the natural history of individual DAVFs may range from benign to life-threatening. Aggressive DAVFs that require urgent treatment include those with cortical or leptomeningeal venous drainage, those with variceal or aneurysmal dilatation, and DAVFs with deep galenic drainage.124 Because of this heterogeneity, management may involve an expectant approach, endovascular therapy, microsurgery, SRS, or a combination of these. SRS has a role in treating selected low-risk DAVFs125 and highrisk DAVFs in which surgery and endovascular therapy have either failed or are not possible because of inaccessibility or patient comorbidities.126 Case series have shown DAVF obliteration rates

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ranging from 68% to 72% with SRS.127,128 As with AVMs, SRS for DAVFs has a latency period during which patients remain at risk for hemorrhage. As a result, surgical resection is the optimal therapy for high-risk DAVFs because of their significantly high annual hemorrhage rates.125-130 If surgical management is not feasible, then we believe the best management option is SRS associated with perioperative embolization to the entire fistula volume. This combination combines the early benefit associated with embolization and the later benefit provided by SRS. Advances in microcatheter technology and our ability to perform superselective angiography may also play increasingly important roles in the treatment of DAVFs. Superselective angiography allows characterization of the angioarchitecture of these complex lesions. Better understanding of the vascular anatomy allows enhanced SRS target definition and may translate into higher obliteration rates with lower associated morbidity.131-133

CONCLUSION For institutions with expertise in AVMs and DAVFs, the continued challenge will be to provide a treatment strategy that can achieve an optimal outcome while minimizing patient morbidity. As we advance our understanding of these lesions, inevitably more and more treatment modalities and various forms of combination therapy will be at our disposal. However, in the face of continued uncertainty regarding the natural history of these lesions, optimal treatment strategies will likely remain highly individualized. Disclosure The authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.

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Advances in radiosurgery for arteriovenous malformations of the brain.

Arteriovenous malformations of the brain are a considerable source of morbidity and mortality for patients who harbor them. Although our understanding...
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