- Department of Neurosurgery, Louisiana State University Health Sciences Center, New Orleans, Louisiana, USA
- Goodman Campbell Brain and Spine, Department of Neurological Surgery, Indiana University School of Medicine, Indianapolis, Indiana, USA
- University of California San Francisco, San Francisco, California, USA
Aaron A. Cohen-Gadol
Goodman Campbell Brain and Spine, Department of Neurological Surgery, Indiana University School of Medicine, Indianapolis, Indiana, USA
DOI:10.4103/2152-7806.153707Copyright: © 2015 Conger A. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
How to cite this article: Conger A, Kulwin C, Lawton MT, Cohen-Gadol AA. Endovascular and microsurgical treatment of cerebral arteriovenous malformations: Current recommendations. Surg Neurol Int 19-Mar-2015;6:39
How to cite this URL: Conger A, Kulwin C, Lawton MT, Cohen-Gadol AA. Endovascular and microsurgical treatment of cerebral arteriovenous malformations: Current recommendations. Surg Neurol Int 19-Mar-2015;6:39. Available from: http://sni.wpengine.com/surgicalint_articles/endovascular-microsurgical-treatment-cerebral-arteriovenous-malformations-current-recommendations/
Background:Cerebral arteriovenous malformations (AVMs) can be a heterogeneous pathological entity whose management requires a complex decision-making process due to the risks associated with their treatment and natural history. Despite the recently published conclusions of the aborted Randomized Trial of Brain Unruptured AVMs (ARUBA) trial, the authors of this article believe multimodality intervention in general and microsurgical resection in particular continue to play a major role in the management of carefully selected ruptured or unruptured AVMs.
Methods:The authors provide an overview of their methodology for endovascular intervention and microsurgical resection and share their technical nuances for successful embolization and microsurgical resection of AVMs with special emphasis on complication avoidance.
Results:The authors have achieved successful outcomes in embolization and resection of cerebral AVMs when using their methodology.
Conclusions:These lesions are among the most technically difficult pathological entities handled by the cerebrovascular specialist, and an overview of technical concepts to help systematize this challenging and variable endeavor can improve the safety of their treatment.
Brain arteriovenous malformations (AVMs) occur in about 0.02% of the adult population.[
Treatment of AVMs is intended to improve upon the natural history of the lesion. However, treatment carries a risk of complications, and short-term data from the aborted Randomized Trial of Brain Unruptured AVMs (ARUBA) trial suggest that treatment does not improve upon the natural history.[
Most AVMs are diagnosed following the acute onset of symptoms consistent with intracerebral hemorrhage such as headaches and neurological changes secondary to rupture of the lesion. A smaller percentage of AVMs are diagnosed during investigation of focal neurologic deficits, seizures, or headaches.[
Traditionally, endovascular treatment of brain AVMs has served an adjunctive role intended to facilitate microsurgical resection or radiosurgical treatment. As a curative measure, embolization has not proven effective, and the obliteration rates of approximately 13%[
In 2010, Feliciano et al. reviewed and analyzed the existing literature on embolization of AVMs.[
If a high-grade AVM is not considered safe for any type of curative treatment, embolization may serve as a way to decrease rupture risk by treating specific features associated with hemorrhage such as nidal aneurysms or venous ectasia.[
By far the most common use of endovascular embolization at our center is as an adjuvant therapy, facilitating microsurgical resection or stereotactic radiosurgery. Embolization prior to stereotactic radiosurgery has been performed as a way of decreasing the size of the nidus and thus the requisite radiation dose.[
At our center, embolization has proven most useful as an adjunct to surgical resection. Embolization is useful for decreasing flow through an AVM and for occluding deep arterial feeders that may be difficult to access microsurgically or those accessible only at the end of dissection.[
As a result, some centers prefer to embolize within as little as 24 h of surgery to minimize assumed increased rupture risk after partial embolization, while other centers wait as long as 3 weeks to allow for stabilization of these hemodynamic changes and presumably easier surgical resection.[
It has been the experience of one of our senior author (ACG) that overembolization of an AVM may lead to more technical difficulty during its resection. Overembolization of the majority of the large pedicles leads the AVM to recruit deep white matter feeders to continue arteriovenous shunting. Such expansion of deep white matter feeders [
Because of the varied applications of endovascular embolization in the treatment of cerebral AVMs, it is recommended that development of the treatment plan for an AVM patient includes the input of an endovascular specialist in conjunction with the microsurgeon and that the specific goals of embolization as determined at the outset as this will determine the approach.[
Once goals of endovascular therapy have been determined, there are a few technical nuances worth further emphasis and consideration. The starting point for embolization is a stable catheter platform anchored in a cervical vessel. A microcatheter is then passed through this platform and selection of arterial feeders can proceed. Direct nidal feeders are ideal for embolization as all of the embolic material will accumulate in the nidus. En passage vessels must be embolized with great care as the embolic material can reflux into the parenchymal branch of the vessel causing an infarction. Arterial and venous compartments may be connected by either a nidal or fistulous connection. Nidal connections are more amenable to safe embolization than fistulous connections that allow embolic material to rapidly traverse to the venous side and may result in occlusion of a draining vein. This is more likely in AVMs with a single draining vein.
In most cases, liquid embolic agents are used for the treatment of AVMs. Two commonly used varieties are cyanoacrylates and ethylene vinyl alcohol (EVOH). Cyanoacrylates are adhesive monomers that polymerize in contact with ionic compounds, resulting in vessel occlusion and the induction of a chronic inflammatory response.[
Once an AVM patient is selected for microsurgery, further imaging evaluation determines the best operative plan. Additional time is committed to deriving all information available from the preoperative angiogram sequences, which are studied at length before surgery. One of the senior authors (MTL) has proposed a “box” concept for analyzing AVMs; this concept assigns six surfaces to each AVM: A superficial plane, a deep plane, and four sides. Successful resection of an AVM requires dissection of these six surfaces.[
Classic angioarchitecture of a frontal AVM. The draining vein, arterial feeders, and a feeding vessel aneurysm are shown. Note the extension of the AVM to the level of the ventricle and the feeding arteries in the periventricular region. A complete resection of a periventricular AVM often requires exposure of the ventricle. Copyright The Neurosurgical Atlas, Aaron A. Cohen-Gadol, MD, MSc. Used with permission
The operation is performed with the surgeon in the sitting position using an armrest. The surgeon's comfort prevents fatigue and provides smooth microsurgical dissection maneuvers during the critical portions of the case. These critical steps often occur later in the case when fatigue can be present. The initial dissection may be performed with loupes to prevent working into a deep hole, but as the dissection proceeds deeper, the microscope is used with the mouthpiece to minimize redundant and nondeliberate movements such as using the microscope handles to refocus the microscope. The mouthpiece is critical for microsurgical efficiency. Monitors showing the oculars’ view should be available to the other members of the operating room team to allow them to follow the procedure and inform them regarding the dissecting instruments needed for the next step.
Irrigating bipolar forceps of various lengths and tips are an important tool for dissection. The irrigation and coagulation levels of this device must be appropriately balanced to prevent accumulation of char on the tips. The tips of bipolars may be kept in cold saline solution to minimize charring of their tips during their use. Next, a variety of dissecting instruments are needed. The width of the tip of dissectors should be matched to the level of microdissection. The angled dissectors provide more flexibility in working around the corners as all the dissection is performed under direction visualization. Blunt and blind dissection is the cause of significant morbidity because of perforator injuries and unintended parenchymal transgressions. Small aneurysm clips may be used to control bleeding from white matter feeders that are not amenable to bipolar coagulation.
The administration of general anesthesia and intraoperative monitoring of physiologic parameters during AVM surgery must be a team effort with open communication among the members of the surgical team. Standard noninvasive monitoring is used along with direct arterial pressure monitoring to ensure that the patient's blood pressure is aggressively treated and maintained within designated parameters. Central venous access is used for larger lesions to ensure rapid restoration of fluid and blood volume if necessary. Hemodynamic stability, cerebral perfusion, and management of intracranial pressure are critically important for maximizing patient outcomes, and anesthetic agents should be selected with these parameters in mind while not interfering with neuromonitoring. Intraoperative hypotension can be used to decrease blood loss and facilitate surgical resection; however, it should be used with caution as hypotension can cause ischemia in parenchyma already subject to hypoperfusion due to arteriovenous shunting. Emergence from anesthesia can often be associated with coughing and bucking, causing periodic increases in intracranial pressure and rebleeding, so after difficult operations associated with high blood loss, large AVMs, or any other concern for postoperative bleeding, the patient remains intubated and sedated overnight to avoid these potential complications.[
As discussed previously, thoughtful positioning of the patient during surgery can facilitate resection by allowing the use of gravity retraction. This is facilitated by referring to the AVM subtypes as described by one of our authors (MTL).[
Common mistakes during patient positioning include failure to use free surfaces to access the lesion and maximize gravity retraction. As a result, fixed retractors may become necessary, risking cortical injury and potentially increasing morbidity. Due to the risk of intraoperative bleeding and technical challenges involved in AVM surgery, the operative corridor has to be generous and provide numerous working angles that are flexible to allow timely handling of subcortical bleeding. Finally, patient positioning should take into account operative routes that will minimize any risk to venous drainage of the AVM.
We use neuronavigation based on MRI data to perform a wide craniotomy in order to expose the AVM nidus, its associated feeding arteries and draining veins, and a region of normal brain surrounding the AVM. If possible, the craniotomy is planned to provide exposure and early opening of cerebrospinal fluid (CSF) cisterns to relax the brain. If this is impractical, we recommend a lumbar drain to gradually drain CSF to provide brain relaxation. A greater number of burr holes and short passes with the craniotome decrease the risk of injury to dilated draining veins that may be traveling in the parasagittal dural leaves and venous lakes. Any violation of the dura during the use of a footplate increases the risk of unintended injury to the draining veins. The avoidance of this complication can be difficult because the engorged draining veins within the dural leaves are often large enough to erode the inner table of the calvarium. The use of the lumbar drain can facilitate thorough dissection of the decompressed dura away from the inner surface of the calvarium. After the craniotomy, a wide durotomy is made [Figures
Following the initial exposure, some surface AVMs are readily visualized, while others are obscured by thickened, possibly hemosiderin-stained arachnoid. A draining vein at the surface may herald the path to a deep lesion, whereas others require detection of more subtle surface cues such as small arterialized veins or mildly dilated arterial feeders, either of which can be traced down a sulcus and ultimately to the AVM nidus. Subarachnoid dissection is an important step in laying out the anatomy of the AVM and securing proximal control [
Arachnoid membranes covering the AVM are often thickened and should be generously dissected open to allow for clear identification of margins of the AVM's free surface and surrounding vessels. Embolized vessels and neuronavigation further assist with delineation of the AVM's margins. Copyright The Neurosurgical Atlas, Aaron A. Cohen-Gadol, MD, MSc. Used with permission
While we continue to dissect the subarachnoid membranes, a thorough review of the preoperative angiogram is performed, correlating the anatomic findings seen in the surgical field to the angiogram. This helps us distinguish between arteries and veins, defines the major draining vein, and determines if arteries are terminal or en passage. The angiogram discloses the compactness of margins and readily visualizes embolic material, allowing its use as a surgical landmark and navigation tool. As discussed previously, detailed study of the preoperative angiogram is essential for successful AVM surgery: This intraoperative review of the angiogram should be a recognition of details already learned, rather than a discovery of new data.[
Defining the draining vein
The fundamental principle of AVM surgery is identification and preservation of the draining vein until all arterial feeders are occluded. Failure to do so results in increased nidal pressure, intraoperative rupture of the AVM, and profuse bleeding from multiple sites along the adjacent normal brain. As the dissection of the arachnoid planes is completed, the distinction of arteries from veins is undertaken.
Determination of the AVM subtype helps predict the expected location of feeding arteries and draining veins, and potentially assists in discerning between the two.[
Once identified, the draining vein is protected throughout the remainder of dissection. Veins are kept irrigated and unstretched, and dissection proceeds on each side of the vein, connecting the developed planes beneath it, but maintaining visualization of the vein so that an instrument passed into the field does not cause its unintended injury. Common mistakes during this part of the operation include failure to distinguish arteries and veins, and inadvertent injury or occlusion of a major draining vein by not being mindful of its presence in the field.
Occluding arterial feeders
After identification of the draining veins, arterial feeders can be identified and occluded [
A surface arterial feeder is identified and occluded using bipolar electrocautery. Cortical and sulcal feeding arteries are readily amenable to bipolar coagulation and allow efficient AVM disconnection at this step of the operation. All cortical veins should be carefully protected at this stage. Copyright The Neurosurgical Atlas, Aaron A. Cohen-Gadol, MD, MSc. Used with permission
Before any artery is occluded, it must be identified as a terminal, en passage, or bystander vessel. We perform this maneuver through safely tracing the arteries proximally and distally to the AVM; we exercise patience and do not get distracted or stressed by bleeding from the AVM. Terminal vessels contribute only to the AVM and do not continue beyond the nidus. En passage vessels contribute branches to the AVM nidus as they pass on their way to supply brain parenchyma. Bystander vessels are near the AVM, but do not contribute any blood flow to it. Bystander and en passage vessels can be distinguished from each other by tracing them, beginning distal to the AVM and working in a proximal direction. Branches contributing to the AVM nidus are coagulated and divided as they identify the en passage vessel. Absence of any contributions to the AVM nidus identifies bystander vessels, which are then protected with cottonoids. Occlusion of large and very small arterial feeders usually requires clips, whereas medium to small arteries can be coagulated over a length of about 5 mm in a proximal-to-distal direction as close to the AVM nidus as possible. Indiscriminate sacrifice of vessels around the AVM to control bleeding of an unknown source leads to brain ischemia and patient morbidity.
A small number of AVMs, such as sylvian AVMs, exist entirely within the subarachnoid space, so exposure is complete after subarachnoid dissection; however, most AVMs require transgression of the pia mater for complete dissection. The pial incision is made tightly around the surface of a cone-shaped AVM, whereas it is wider around a sphere-shaped AVM, often requiring resection of some overlying cortex to prevent overhanging tissue that limits visualization and risks incomplete resection. Great care is taken to protect areas of eloquence by keeping the pial incision and subsequent dissection plane as near the AVM as possible along the edges adjacent to eloquent brain. Arterial feeders encountered on the pial surface are divided as the pial incision is made circumferentially around the AVM. These lesions do not conform to regular shapes, therefore it is important not to enter the AVM during this step of resection. Entering the nidus often leads to excessive bleeding and alerts the surgeon to stay on the outside border of the lesion.
Dissection proceeds into the parenchyma and follows the edge of the nidus around in a circumferential manner [
Presence of a parenchymal hematoma eases this stage of the operation because it provides a parenchymal corridor that is used during dissection of the AVM. The hemorrhage has already caused neurologic morbidity, decreasing the risk of iatrogenic morbidity as that area's eloquence has been removed from the equation.
As dissection proceeds around the AVM, white matter arterial feeders are often encountered; some of the more superficial ones are amenable to occlusion using bipolar coagulation [
Deep arterial feeders may be clipped and divided as they do not easily occlude with bipolar coagulation. When not in use, bipolar forceps may be kept in ice saline to minimize charring at their tips during their application. Copyright The Neurosurgical Atlas, Aaron A. Cohen-Gadol, MD, MSc. Used with permission
We also use broad bipolar tips on a low setting during this stage of dissection. Keeping the bipolar tips cold (in ice saline) aids in dissection of these vessels by preventing the tips from becoming sticky. For larger AVMs, these deep arteries are often more problematic because some draining veins have been divided by this point in the operation, causing the remaining arterial feeders to be under high pressure. In select AVMs with angiographically known deep feeders (enlarged lenticulostriate arteries), we have alleviated this problem by dissecting down to the deepest portion of the AVM first (rather than circumdissection) and dividing these deep feeders early during the operation. However, this technique is not widely agreed upon among AVM surgeons.
Dissection of the deep plane of the AVM is the most difficult. This area of dissection lies at the depths of the resection cavity [
Parenchymal dissection and division of deep arterial feeders proceed toward the ventricle. If bleeding is encountered, the small deep veins and choroidal feeding vessels are coagulated and divided. All arterialized veins are protected until the last stage of the operation. Copyright The Neurosurgical Atlas, Aaron A. Cohen- Gadol, MD, MSc. Used with permission
After dissection of the AVM is complete, the draining vein should be noticeably blue, indicating an absence of arterial input. Persistent red color within the vein necessitates inspection for an arterial feeder that was missed. Most commonly an arterial feeder is hidden under the draining vein or a remnant was left in a difficult-to-visualize area of the resection cavity. The draining vein may be temporarily occluded to ensure no swelling within the AVM. If it is unclear whether the arterial supply has been completely occluded, indocyanine green can be administered. No fluorescent signal should be detected within the draining vein. At this point, the AVM nidus is rolled out of the resection cavity attached to its venous pedicle. The draining vein is then coagulated or clipped and divided [
The AVM is removed from the resection cavity, which is inspected for any persistent bleeding. Often, aggressive coagulation should be avoided since the brain may be quite friable. We irrigate the resection cavity with thrombin solution and exercise patience. Copyright The Neurosurgical Atlas, Aaron A. Cohen-Gadol, MD, MSc. Used with permission
The technical nuances for AVM resection are illustrated in
The patient is admitted to the intensive care unit after surgery and his or her systolic blood pressure is kept below what is normal for the patient (~100–120 mm/Hg). The patient is closely observed for evidence of postoperative bleeding. After difficult cases, large AVMs, presence of intraoperative swelling, or any case that causes concern for postoperative hemorrhage, the patient is kept intubated and sedated overnight to prevent the blood pressure spikes that often accompany coughing and gagging during extubation. A postoperative CT and angiogram is obtained on postoperative day 1. If any AVM remnant is observed, the patient is returned for reoperation immediately or as soon as the patient is deemed safe to return to surgery. Pediatric AVMs are notorious for their recurrence, partly due to their noncompact nidus, and must undergo surveillance imaging for years after surgery.
Resection or embolization of AVMs can be marred by many complications, including neurologic deficits from overly aggressive dissection or ischemic infarcts, seizures, hydrocephalus, and infection; however, three complications deserving specific consideration are intraoperative rupture, postoperative hemorrhage, and postoperative edema.
Intraoperative AVM rupture is a potentially disastrous consequence of premature occlusion of one or more major draining veins. This complication is usually a result of mistaking numerous smaller arterialized veins for feeding arteries and occluding them, although it can be caused by inadvertent occlusion of the prominent draining vein. This sometimes occurs during attempts to regain hemostasis after the draining vein is injured or by kinking of the vein while the nidus is held in fixed retraction. This can also occur during attempted embolization of a high-flow fistula. All of these unfortunate events are more likely in the event of heavy bleeding and pressured decision-making, underscoring the importance of maintaining hemostasis throughout the dissection.
Residual AVM nidus may lead to bleeding within the adjacent normal brain, leading to intraoperative brain swelling. Once a significant portion of the AVM outflow has been compromised, the nidus swells, arterial feeders engorge and become less responsive to coagulation, and areas of the nidus begin to spontaneously bleed. At this point, careful, methodical dissection is no longer an option, and an operation ensues that we refer to as “commando resection.”[
Severe edema and hemorrhage are the two most common postoperative complications after resection or embolization of large AVMs. The exact etiology of these complications remains unclear, but is almost certainly a result of altered hemodynamics in the wake of AVM resection. Two explanations have been reported. Spetzler et al. attributed these phenomena to normal perfusion pressure breakthrough, asserting that the arterioles surrounding an AVM have been exposed to low perfusion pressures and are maximally vasodilated.[
Regardless of the cause, these complications are more common with larger AVMs and with AVMs with high-flow shunting. They can often be minimized or avoided by gradual embolization of portions of the AVM before surgery to allow the surrounding brain to accommodate for hemodynamic changes that ensue after sudden AVM resection. In other words, this is often staged to allow blood flow to return to hypoperfused regions in a piecemeal fashion, rather than all at once following resection. Managing the altered hemodynamics in this staged manner decreases the incidence of these postoperative complications. If edema or hemorrhage develops postoperatively despite meticulous blood pressure control, it can be effectively managed medically with hypertonic therapies or, if necessary, a ventriculostomy to drain CSF and decrease intracranial pressure.
Microsurgical resection remains the ideal treatment for many cerebral AVMs. It is a definitive and immediate cure for a potentially devastating pathology. Resection can often be facilitated by endovascular embolization, and in carefully selected cases, embolization may be a curative treatment on its own. Although AVM treatment can be fraught with complications and morbidity, the combination of judicious patient selection, tireless assessment of all preoperative data, meticulous technical skill, and the humility of the clinician to recognize, correct, and learn from one's mistakes results in favorable outcomes for management of one of the most daunting cerebrovascular lesions.The technical nuances for AVM resection are illustrated in Video 1 (available on the World Wide Web at https://www.youtube.com/watch?v=WA2FTX1NK1Y)
1. Al-Rodhan NR, Sundt TM, Piepgras DG, Nichols DA, Rufenacht D, Stevens LN. Occlusive hyperemia: A theory for the hemodynamic complications following resection of intracerebral arteriovenous malformations. editors. J Neurosurg. 1993. 78: 167-75
2. Al-Shahi R, Fang JS, Lewis SC, Warlow CP. Prevalence of adults with brain arteriovenous malformations: A community based study in Scotland using capture-recapture analysis. editors. J Neurol Neurosurg Psychiatry. 2002. 73: 547-51
3. Andrade-Souza YM, Ramani M, Beachey DJ, Scora D, Tsao MN, Terbrugge K. Liquid embolisation material reduces the delivered radiation dose: A physical experiment. editors. Acta Neurochir (Wien). 2008. 150: 161-4
4. Batjer HH, Devous MD, Seibert GB, Purdy PD, Ajmani AK, Delarosa M. Intracranial arteriovenous malformation: Relationships between clinical and radiographic factors and ipsilateral steal severity. editors. Neurosurgery. 1988. 23: 322-8
5. Bendok BR, El Tecle NE, El Ahmadieh TY, Koht A, Gallagher TA, Carroll TJ. Advances and innovations in brain arteriovenous malformation surgery. editors. Neurosurgery. 2014. 74: S60-73
6. Bing F, Doucet R, Lacroix F, Bahary JP, Darsaut T, Roy D. Liquid embolization material reduces the delivered radiation dose: Clinical myth or reality?. editors. AJNR Am J Neuroradiol. 2012. 33: 320-2
7. Blackburn SL, Ashley WW, Rich KM, Simpson JR, Drzymala RE, Ray WZ. Combined endovascular embolization and stereotactic radiosurgery in the treatment of large arteriovenous malformations. editors. J Neurosurg. 2011. 114: 1758-67
8. Feliciano CE, de Leon-Berra R, Hernandez-Gaitan MS, Rodriguez-Mercado R. A proposal for a new arteriovenous malformation grading scale for neuroendovascular procedures and literature review. editors. P R Health Sci J. 2010. 29: 117-20
9. Fullerton HJ, Achrol AS, Johnston SC, McCulloch CE, Higashida RT, Lawton MT. Long-term hemorrhage risk in children versus adults with brain arteriovenous malformations. editors. Stroke. 2005. 36: 2099-104
10. Gross BA, Du R. Natural history of cerebral arteriovenous malformations: A meta-analysis. editors. J Neurosurg. 2013. 118: 437-43
11. Han PP, Ponce FA, Spetzler RF. Intention-to-treat analysis of Spetzler-Martin grades IV and V arteriovenous malformations: Natural history and treatment paradigm. editors. J Neurosurg. 2003. 98: 3-7
12. Hofmeister C, Stapf C, Hartmann A, Sciacca RR, Mansmann U, terBrugge K. Demographic, morphological, and clinical characteristics of 1289 patients with brain arteriovenous malformation. editors. Stroke. 2000. 31: 1307-10
13. Jahan R, Murayama Y, Gobin YP, Duckwiler GR, Vinters HV, Vinuela F. Embolization of arteriovenous malformations with Onyx: Clinicopathological experience in 23 patients. editors. Neurosurgery. 2001. 48: 984-95
14. Kalani MY, Albuquerque FC, Fiorella D, McDougall CG. Endovascular treatment of cerebral arteriovenous malformations. editors. Neuroimaging Clin N Am. 2013. 23: 605-24
15. Kano H, Kondziolka D, Flickinger JC, Park KJ, Iyer A, Yang HC. Stereotactic radiosurgery for arteriovenous malformations after embolization: A case-control study. editors. J Neurosurg. 2012. 117: 265-75
16. Kish KK, Rapp SM, Wilner HI, Wolfe D, Thomas LM, Barr J. Histopathologic effects of transarterial bucrylate occlusion of intracerebral arteries in mongrel dogs. editors. AJNR Am J Neuroradiol. 1983. 4: 385-7
17. Klara PM, George ED, McDonnell DE, Pevsner PH. Morphological studies of human arteriovenous malformations. Effects of isobutyl 2-cyanoacrylate embolization. editors. J Neurosurg. 1985. 63: 421-5
18. Klurfan P, Gunnarsson T, Haw C, Ter Brugge KG. Endovascular treatment of brain arteriovenous malformations: The Toronto experience. editors. Interv Neuroradiol. 2005. 11: 51-6
19. Krings T, Hans FJ, Geibprasert S, Terbrugge K. Partial “targeted” embolisation of brain arteriovenous malformations. editors. Eur Radiol. 2010. 20: 2723-31
20. Kusske JA, Kelly WA. Embolization and reduction of the “steal” syndrome in cerebral arteriovenous malformations. editors. J Neurosurg. 1974. 40: 313-21
21. Lawton MT. Seven AVMs: Tenets and Techniques for Resection. editors. New York: Thieme Medical Publishers; 2014. p.
22. Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL. A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. editors. Neurosurgery. 2010. 66: 702-13
23. Le Feuvre D, Taylor A. Target embolization of AVMs: Identification of sites and results of treatment. editors. Interv Neuroradiol. 2007. 13: 389-94
24. Luessenhop AJ, Mujica PH. Embolization of segments of the circle of Willis and adjacent branches for management of certain inoperable cerebral arteriovenous malformations. editors. J Neurosurg. 1981. 54: 573-82
25. Meisel HJ, Mansmann U, Alvarez H, Rodesch G, Brock M, Lasjaunias P. Effect of partial targeted N-butyl-cyano-acrylate embolization in brain AVM. editors. Acta Neurochir (Wien). 2002. 144: 879-87
26. Miller C, Mirski M. Anesthesia considerations and intraoperative monitoring during surgery for arteriovenous malformations and dural arteriovenous fistulas. editors. Neurosurg Clin N Am. 2012. 23: 153-64
27. Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): A multicentre, non-blinded, randomised trial. editors. Lancet. 2014. 383: 614-21
28. Morris Z, Whiteley WN, Longstreth WT, Weber F, Lee YC, Tsushima Y. Incidental findings on brain magnetic resonance imaging: Systematic review and meta-analysis. editors. BMJ. 2009. 339: b3016-
29. Murayama Y, Vinuela F, Ulhoa A, Akiba Y, Duckwiler GR, Gobin YP. Nonadhesive liquid embolic agent for cerebral arteriovenous malformations: Preliminary histopathological studies in swine rete mirabile. editors. Neurosurgery. 1998. 43: 1164-75
30. Natarajan SK, Born D, Ghodke B, Britz GW, Sekhar LN. Histopathological changes in brain arteriovenous malformations after embolization using Onyx or N-butyl cyanoacrylate. Laboratory investigation. editors. J Neurosurg. 2009. 111: 105-13
31. Natarajan SK, Ghodke B, Britz GW, Born DE, Sekhar LN. Multimodality treatment of brain arteriovenous malformations with microsurgery after embolization with onyx: Single-center experience and technical nuances. editors. Neurosurgery. 2008. 62: 1213-25
32. Ogilvy CS, Stieg PE, Awad I, Brown RD, Kondziolka D, Rosenwasser R. AHA Scientific Statement: Recommendations for the management of intracranial arteriovenous malformations: A statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. editors. Stroke. 2001. 32: 1458-71
33. Potts MB, Jahangiri A, Jen M, Sneed PK, McDermott MW, Gupta N. Deep arteriovenous malformations in the Basal Ganglia, Thalamus, and Insula: Multimodality management, patient selection, and results. editors. World Neurosurg. 2014. 82: 386-94
34. Pradilla G, Coon AL, Huang J, Tamargo RJ. Surgical treatment of cranial arteriovenous malformations and dural arteriovenous fistulas. editors. Neurosurg Clin N Am. 2012. 23: 105-22
35. Richling B, Killer M, Al-Schameri AR, Ritter L, Agic R, Krenn M. Therapy of brain arteriovenous malformations: Multimodality treatment from a balanced standpoint. editors. Neurosurgery. 2006. 59: S148-57
36. Saatci I, Geyik S, Yavuz K, Cekirge HS. Endovascular treatment of brain arteriovenous malformations with prolonged intranidal Onyx injection technique: Long-term results in 350 consecutive patients with completed endovascular treatment course. editors. J Neurosurg. 2011. 115: 78-88
37. Sanborn MR, Park MS, McDougall CG, Albuquerque FC. Endovascular approaches to pial arteriovenous malformations. editors. Neurosurg Clin N Am. 2014. 25: 529-37
38. Schwyzer L, Yen CP, Evans A, Zavoian S, Steiner L. Long-term results of gamma knife surgery for partially embolized arteriovenous malformations. editors. Neurosurgery. 2012. 71: 1139-47
39. Shtraus N, Schifter D, Corn BW, Maimon S, Alani S, Frolov V. Radiosurgical treatment planning of AVM following embolization with Onyx: Possible dosage error in treatment planning can be averted. editors. J Neurooncol. 2010. 98: 271-6
40. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. editors. J Neurosurg. 1986. 65: 476-83
41. Spetzler RF, Wilson CB, Weinstein P, Mehdorn M, Townsend J, Telles D. Normal perfusion pressure breakthrough theory. editors. Clin Neurosurg. 1978. 25: 651-72
42. Starke RM, Meyers PM, Connolly ES. Adjuvant endovascular management of brain arteriovenous malformations. Winn R, editors. Youmans Neurological Surgery. 2011. p.
43. Taylor CL, Dutton K, Rappard G, Pride GL, Replogle R, Purdy PD. Complications of preoperative embolization of cerebral arteriovenous malformations. editors. J Neurosurg. 2004. 100: 810-2
44. van Beijnum J, van der Worp HB, Buis DR, Al-Shahi Salman R, Kappelle LJ, Rinkel GJ. Treatment of brain arteriovenous malformations: A systematic review and meta-analysis. editors. JAMA. 2011. 306: 2011-9
45. van Rooij WJ, Jacobs S, Sluzewski M, van der Pol B, Beute GN, Sprengers ME. Curative embolization of brain arteriovenous malformations with onyx: Patient selection, embolization technique, and results. editors. AJNR Am J Neuroradiol. 2012. 33: 1299-304
46. Vinuela F, Duckwiler G, Jahan R, Murayama Y. Therapeutic management of cerebral arteriovenous malformations. Present role of interventional neuroradiology. editors. Interv Neuroradiol. 2005. 11: 13-29
47. Yu SC, Chan MS, Lam JM, Tam PH, Poon WS. Complete obliteration of intracranial arteriovenous malformation with endovascular cyanoacrylate embolization: Initial success and rate of permanent cure. editors. AJNR Am J Neuroradiol. 2004. 25: 1139-43