The authors thank all the clinical teams contributing daily to the care of AVM patients at UCSD.

All procedures described below are performed as standard of care for patients with cerebral AVMs, after obtaining informed consent as per institutional guidelines.
1. Initial patient evaluation and imaging
NOTE: Patients with unruptured AVMs often present after the malformation is discovered on imaging for headache or seizure workup. Patients with ruptured AVMs often present with acute onset of headache, nausea, vomiting, weakness, numbness, and/or vision changes.
<ol>
	<li>Obtain a thorough history by interviewing the patient and/or family (to determine previous rupture status, family history) and perform a detailed neurologic exam evaluating level of consciousness and orientation, cranial nerve function, extremity motor and sensory function, and reflexes. This exam may identify neurologic deficits as a result of occult vascular steal, local mass effect, and/or visual changes (with occipital AVMs). In cases of an AVM rupture, admit the patient to the intensive care unit (ICU), and care for according to American Heart Association (AHA)/American Stroke Association (ASA) guidelines in conjunction with the neurocritical care team.9</li>
	<li>Obtain a non-contrast head computed tomography (CT) per institutional protocol to evaluate for acute hemorrhage, i.e., an area of abnormal intracranial hyperdensity, often with mass effect. Obtain vascular imaging via CT- or magnetic resonance (MR)-angiography per institutional protocol to define cerebral vasculature and any underlying vascular abnormalities.10 Perform interpretation of all images by neurosurgical and radiology teams.</li>
	<li>If the patient is neurologically stable, obtain informed consent and book the patient for definitive vascular imaging via six-vessel catheter angiography &#177; embolization (see sections 2 and 3 below). If the patient has progressive neurologic decline from a hemorrhage, place an intracranial pressure monitor and/or initiate osmotic therapies in accordance with AHA/ASA guidelines9. Pursue hematoma evacuation &#177; AVM resection (see section 4 below) prior to or immediately following diagnostic six-vessel catheter angiography.</li>
</ol>
2. Six-vessel angiography
<ol>
	<li>Position the patient supine on the fluoroscopy table after administration of a light sedative if stable, or under general anesthesia if unstable with assistance from the anesthesiology team (typical induction for intubation with fentanyl [5-10 ucg/kg], midazolam [0.2-0.4 mg/kg], and 0.5 mg/kg rocuronium, followed by anesthesia maintenance with propofol at 50 -150 ucg/kg/min and remifentanil at 0.1-0.5 ucg/kg/min).11</li>
	<li>Place a right femoral artery sheath using a micropuncture groin access kit and a modified Seldinger technique.12
	<ol>
		<li>Clean (with 2% chlorhexidine gluconate and 70% isopropyl alcohol) and sterilely drape the groin.</li>
		<li>Palpate the femoral artery at the inguinal crease. Inject 1-2 mL of 1% Lidocaine HCl as a local anesthetic into the superficial subcutaneous tissue. Insert the micro-needle into the femoral artery lumen with the needle at a 45&#176; angle to the skin.</li>
		<li>Advance a micro-wire through the micro-needle, and remove the micro-needle keeping the micro- wire in place. Make a 0.5cm skin puncture with a # 11 blade at site of microwire exiting skin.</li>
		<li>Insert a vessel dilator, and then remove the micro-wire and inner portion of the vessel dilator, keeping the outer portion of the vessel dilator in place.</li>
		<li>Insert a J-wire through the lumen of the vessel dilator, and remove the vessel dilator, keeping the J-wire in place.</li>
		<li>Insert a 5 or 6-French sheath over the J-wire into the femoral artery. Remove the J-wire, keeping the sheath in place in the artery.</li>
	</ol>
	</li>
	<li>Advance a 0.035 guidewire and 4-French diagnostic catheter cephalad under mono- or biplane fluoroscopy (3-5 frames per second) to the ascending aorta, and selectively catheterize and image via injection of 5-8 mL of radio-opaque contrast agent (240 mg/mL) the right external and internal carotid arteries, the right vertebral artery, the left internal carotid artery, the left external carotid artery, and the left vertebral artery.</li>
	<li>Review recorded angiographic images of the above vessel runs to determine the feeding vessels and draining veins of the AVM.</li>
	<li>If acute embolization not pursued, remove the diagnostic catheter and guidewire, and secure the femoral artery with a sealant device as per manufacturer instructions,13 or by holding pressure for at least 10 min.</li>
</ol>
3. AVM embolization
NOTE: If the AVM is amenable to endovascular and subsequent surgical treatment (as defined by established grading scales1,8 as well as surgeon and multidisciplinary conference evaluations), the initial embolization may be performed in a delayed fashion or in the same session as the diagnostic angiography. Embolizations are often staged to decrease rupture and stroke risk from rapidly altered flow dynamics.
<ol>
	<li>Obtain informed consent. With assistance from anesthesia place the patient under general anesthesia as in 2.1, and position the patient supine on the fluoroscopy table (if not at same time as initial angiogram).</li>
	<li>In conjunction with a neuro-monitoring team, establish baseline neuromonitoring via somatosensory evoked potentials (SSEPs), transcranial motor evoked potentials (TcMEPs), visual evoked potentials (VEPs), auditory brainstem responses (ABRs), and/or electroencephalography (EEG). Continue neuro-monitoring throughout the case to track in real-time the function of critical neural pathways. SSEPs, TcMEPs, and EEG are used as part of a standard neuro-monitoring protocol, with addition of ABRs for vertebral/basilar artery lesions, and VEPs for visual cortex lesions.14</li>
	<li>Obtain femoral arterial access utilizing the modified Seldinger technique and insert a 6- French femoral sheath as in 2.2.</li>
	<li>Introduce a pre-assembled co-axial system consisting of a 6-French guide catheter (a larger bore catheter on the outside of the system for stabilization), a 4-French diagnostic catheter (a smaller bore catheter positioned inside the 6-French guide for selective vessel catheterization), and a 0.035 guidewire (positioned within the lumen of the 4-French diagnostic catheter for system guidance) as one unit into the femoral sheath.</li>
	<li>As in 2.3 advance the co-axial system cephalad and selectively catheterize the large-caliber cervical vessel (i.e. left or right internal carotid or vertebral artery) from which the desired feeding AVM vessel originates with the diagnostic catheter and advance the guide catheter to the appropriate cervical segment for support. Remove the diagnostic catheter, ensure adequate vessel runoff via rapid dispersion of a small injection of contrast, and perform a diagnostic angiogram (under mono- or biplane fluoroscopy, 3-5 frames per second) by injection of radio-opaque contrast (5-8 mL of 240 mg/mL)&#160;to assess the blood supply of the AVM. An overlay guidance image (superimposition of desired vessel run with real-time fluoroscopy) or roadmap image (vessel subtraction template) is then created to assist with micro-catheterization of the target AVM vessel.</li>
	<li>Introduce a dimethyl-sulfoxide (DMSO) compatible microcatheter and microwire into the guide catheter at the groin, and advance the cephalad to selectively catheterize the desired feeding artery using overlay or roadmap guidance.</li>
	<li>Once the embolization position is reached with the microcatheter it is flushed with (DMSO). Once flushed, embolize the AVM nidus and desired feeding artery via controlled injection of a radio-opaque liquid embolic agent under a negative roadmap image until reflux tolerance is reached. Total volume of embolisate used is dictated by the size of the lesion, penetration of the nidus, and allowable reflux. Take care to avoid embolisate reflux into non-AVM arteries, or distal embolization into draining veins. Once the embolization is complete, back aspiration on the embolization syringe is held and the catheter is removed under fluoroscopic visualization.</li>
	<li>Repeat as needed by catheterizing other feeding vessels, with a goal of at least 50% pre-operative nidal embolization.15 Generally, only one or two feeding vessels and &#60;40% of the nidus are embolized in a single procedure, making staged embolizations common.</li>
	<li>Perform final vascular imaging by contrast injection through the guide catheter as in step 3.5 to evaluate the AVM embolization and ensure patency of parent vessels.</li>
	<li>Withdraw the guide catheter and close the femoral artery as in step 2.5. If the patient is being taken directly to the OR for resection, the femoral sheath may be left in place for intra-operative angiogram (described in step 4.8).</li>
</ol>
4. AVM resection
<ol>
	<li>Obtain informed consent, with assistance from anesthesia place the patient under general anesthesia as in step 2.1, and position the patient based on location of AVM and desired craniotomy. Have blood consent and products available.</li>
	<li>In conjunction with a neuromonitoring team, establish baseline neuromonitoring as described in 3.2, with continued monitoring throughout the case.</li>
	<li>Sync pre-operative imaging with intra-operative neuro-navigation system using surface matching, marker, or pointer registration as per neuronavigation system specifications.</li>
	<li>Obtain groin access as in step 2.2, if sheath is not already in place.</li>
	<li>Perform a craniotomy tailored to the specific AVM location within the cranium using a high-power drill system, ensuring a wide bony exposure.
	<ol>
		<li>Incise the skin and galea using a #15 blade. Obtain hemostasis by placement of Raney clips on the skin edges and/or with Bovie electrocautery using the coagulate setting (Bovie Medical Products, Clearwater, FL). If the planned incision involves underlying muscle, incise the fascia/muscle with electrocautery. Expose the cranium by elevating the incised soft tissue flap from the bone with a periosteal elevator. Alternatively, a pericranial graft can be separately harvested at this time to assist later with closure. Hooks are used for soft tissue retraction.&#160; Irrigate and obtain hemostasis.</li>
		<li>Create one or multiple burr holes on the periphery of the desired craniotomy with a 3 mm diameter matchstick drill bit using a high power drill system. Additional burr holes will allow for shorter bony cuts and for the dura to be stripped multifocally prior to performing the craniotomy.</li>
		<li>Strip the dura locally from the inside of the skull by scraping the inner surface of the bone with a bone elevator or footplate attachment, and complete the craniotomy by connecting the burr holes with a tapered drill bit with a footplate attachment for dural protection. If possible, plan the craniotomy to ensure early access to cerebrospinal fluid (CSF) cisterns for drainage.</li>
		<li>Alternatively, place an external ventricular drain into the lateral ventricle at either Frazier&#39;s or Kocher&#39;s point (after creating a small burr hole as in 4.5.1 and opening the dura sharply using a #11 blade) for CSF drainage. A lumbar drain placed in the lumbar thecal sac following puncture with a large bore Tuohy needle at approximately the L3-L4 or L4-L5 interspace may also be used for CSF drainage.</li>
	</ol>
	</li>
	<li>After removal of the bone flap and obtaining hemostasis through bipolar electrocautery, place dural tack-up sutures to close off the epidural space by drilling small holes in the bone around the craniotomy with a C1 drill bit, and securing the dura to the bone at these sites using 4-0 sutures. Then, open the dura sharply using a #11 or #15 blade. Take great care to not injure the underlying cortex or cortical vessels. Once a small durotomy has been created, open the remaining exposed dura in either a cruciate or c-shaped fashion using Metzenbaum scissors, with Gerald forceps used to elevate the dural edge and visualize the tips of the scissors while cutting to preserve underling cortical structures.</li>
	<li>Using an operating microscope with a variable magnification capacity of approximately 1.5X to 17.0X with a 10X eyepiece, excise the AVM.5 Other forms of surgical magnification, such as an exoscope, can also be used.
	<ol>
		<li>Start microsurgical resection by first dissecting within the subarachnoid space (using a combination of blunt and sharp technique with bipolar forceps, a curved dissector, and microscissors) to define the AVM anatomy and expose its margins, free draining veins, and obtain proximal control by identifying and dissecting free all feeding arteries.</li>
		<li>Take great care to identify and preserve the draining veins early in the AVM dissection, as occlusion of the venous drainage prior to the arterial feeders results in engorgement of the AVM and increased rupture risk.</li>
		<li>After defining this anatomy, coagulate arterial feeding arteries as they enter the AVM in a proximal to distal fashion using bipolar electrocautery by gently holding the vessel between the tips of the bipolar forceps and using up to 30 watts of power, or by the placement of small aneurysm clips.</li>
		<li>Dissect circumferentially within the brain parenchyma immediately around the AVM nidus using bipolar forceps (for dissection and electrocautery) and a variable action suction tip. A brain retractor may be used to facilitate visualization for deep dissections.</li>
		<li>After completion of the AVM dissection, coagulate using bipolar electrocautery as in step 4.7.3 and/or clip any draining veins. Remove the AVM from the resection cavity. It is critical to remove the entire lesion to eliminate future hemorrhage risk.</li>
		<li>If surgical resection is being attempted post-hemorrhage, perform removal of the hematoma remote from the AVM nidus until the brain is decompressed, and feeding vessels and draining veins are identified. After these landmarks are identified, continue AVM nidal resection as in step 4.7.</li>
	</ol>
	</li>
	<li>After AVM removal, perform an intra-operative angiogram as in steps 2.1-2.4, using the arterial sheath placed in step 4.4. Use intraoperative single- or bi-plane angiography or C-arm fluoroscopy to ensure complete nidal resection.</li>
	<li>Obtain meticulous hemostasis using bipolar electrocautery as in step 4.7.4 and by gently lining the resection cavity with absorbable hemostatic agents. Close or re-approximate the dura using 4-0 sutures and, if needed, a peri-cranial or synthetic dural graft. Replace and secure the bone flap using a plating system, and close the galea and skin using interrupted absorbable sutures for the deep layers and either staples or running suture for the skin. Remove the groin sheath and secure the groin as in step 2.5.</li>
	<li>Extubate if able, and transfer the patient to the ICU for close neurologic monitoring and recovery.</li>
</ol>
5. Long term follow up
<ol>
	<li>After a radiographically confirmed complete AVM resection (either via intra-operative or post-operative catheter angiography), obtain remote imaging via catheter angiography at 1- and 5-year post-treatment.</li>
</ol>

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R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Simple+risk+predictions+for+arteriovenous+malformation+hemorrhage.">Simple risk predictions for arteriovenous malformation hemorrhage.</a> Neurosurgery. 37 (5), 851-855 (1995).</li><li>Fukuda, K., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Multicenter+assessment+of+morbidity+associated+with+cerebral+arteriovenous+malformation+hemorrhages.">Multicenter assessment of morbidity associated with cerebral arteriovenous malformation hemorrhages.</a> J Neurointerv Surg. , (2016).</li><li>Conger, A., Kulwin, C., Lawton, M. T., Cohen-Gadol, A. 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AAK holds consulting arrangements for physician training with Covidien. AAK has no direct financial interests related to this work. The remaining authors have no disclosures concerning the materials or methods used in this study or the findings specified in this paper.

Here we demonstrate a comprehensive approach to cerebral AVMs via combined endovascular and open surgical management. Catheter angiography is the gold standard for imaging AVMs, and is critical to surgical evaluation and planning. Pre-operative embolizations can simplify surgical resection, but requires communication between the surgical and interventional teams to develop an optimal strategic approach. For example, the AVM arterial feeders most easily embolized may also be the most surgically accessible. If, however, they are embolized prior to development of a comprehensive treatment plan, leaving only deeper more difficult to access arterial feeders, surgery becomes more difficult without further embolization and exposes the patient to potentially avoidable procedures. 
The main advantage of comprehensively trained neurovascular surgeons is that the same individual is performing all of the above procedures. No two AVMs are exactly alike, and this heterogeneity demands a flexible, individualized treatment approach based on lesion morphology, patient characteristics, and clinical presentation. The above protocol ensures not only that the optimal pre-operative embolization strategy is pursued, but also gives the surgeon an intricate understanding of the lesion before resection is attempted. Additionally, as the risk of venous outflow obstruction and rupture increases with progressive AVM embolizations, this combined approach allows for a planned craniotomy and resection to immediately follow a final aggressive embolization, all during a single anesthesia session. 
Critical steps for complication avoidance within this protocol include: i) appropriate patient selection based on a given AVMs expected natural history versus treatment risks,5,6 ii) selective AVM embolization without compromise of the arterial supply of normal brain (to prevent iatrogenic strokes) or sacrifice of draining veins (to minimize treatment-associated hemorrhage risk), and iii) step-wise surgical resection to avoid massive hemorrhage or damage to surrounding parenchyma. Because the ultimate goal of this combined approach is a safe surgical resection, it is well suited for smaller, more superficial AVMs not involving eloquent cortex. For surgically inaccessible lesions, radiosurgery is often the treatment of choice as opposed to the embolization/surgical resection protocol described herein. 
As evidenced by this multi-step protocol, the treatment of AVMs is complex, and requires cooperation across multiple teams. In addition to the neurovascular surgery team, critical contributions include neuroanesthesia to control intracranial pressure and ensure hemodynamic stability in case of AVM rupture, neuromonitoring to identify in real time neurologic changes and allow appropriate modification of the surgical or endovascular plan, and neurocritical care to help manage the intensive care unit (ICU) needs of these challenging patients. As such, management of AVMs is best undertaken at high-volume centers where this multi-disciplinary infrastructure is in place.

Cerebral arteriovenous malformations (AVMs), abnormal connections between arteries and veins without intervening normal capillary beds, present unique neurosurgical challenges. Classified based on size, presence of deep draining veins, and involvement of eloquent cortex,1 the risk of hemorrhage for previously unruptured AVMs ranges from 0.9 to 8% per year,2 with an annual average rupture risk of ~3%.3 Hemorrhages from AVMs are associated with a nearly 10% mortality rate and significant morbidity, with up to 34% of patients having moderate to severe disabilities.4 Previously ruptured AVMs have increased annual hemorrhage rates,2 but a relatively low immediate risk of re-rupture. Unless mass effect from a hematoma demands acute intervention, treatment is often performed on an elective basis after weighing the expected natural history of a lesion versus its treatment-associated risks.5,6
Surgical resection is the treatment of choice for small accessible AVMs as it immediately and definitively eliminates future hemorrhage risk. However, the high flow rate of AVMs, as well as the increased risk of AVM-associated aneurysms,4,7 makes surgical resection amongst the most challenging of all neurosurgical cases. Pre-operative embolization of AVMs to reduce blood flow and remove high-risk AVM features can significantly reduce the technical challenges of resection.
Comprehensively trained vascular neurosurgeons are uniquely positioned to definitively treat AVMs by performing both the pre-operative angiogram and endovascular embolization, as well as the open surgical resection. Herein, we describe the protocol for management of surgically accessible cerebral AVMs (as defined by established grading scales1,8 as well as surgeon and multidisciplinary conference evaluations) at our institution.

<table><tbody><tr><td>ChloraPrep Sterilization Solution</td><td>BD, Franklin Lakes, NJ</td><td>260815</td><td>For skin sterilization</td></tr><tr><td>Lidocaine Hcl 1%</td><td>ACE Surgical Supply, Inc, Brockton, MA</td><td>001-1421</td><td>For local anesthetic</td></tr><tr><td>Micropuncture Groin Access Kit</td><td>Cook Medical, Bloomington, IN</td><td>G56202</td><td>Used for femoral artery access</td></tr><tr><td>0.035 Guidewire</td><td>Terumo Medical, Somerset, NJ</td><td>GR3506</td><td>Used in conjunction with diagnostic catheters for cerebral angiography</td></tr><tr><td>Cerebral Angiography Diagnostic Catheters</td><td>Terumo Medical, Somerset, NJ</td><td>CG416</td><td>Used in conjunction with guidewire for cerebral angiography</td></tr><tr><td>Omnipaque Contrast Agent</td><td>GE Healthcare, Chicago, IL</td><td>Q9965</td><td>Contrast agent for cerebral vessel imaging</td></tr><tr><td>Microcatheter and Microwire</td><td>Covidian, Plymouth, MN</td><td>105-5091-150, 103-0608</td><td>Used for distal arterial catheterization</td></tr><tr><td>Onyx Liquid Embolic</td><td>Covidian, Plymouth, MN</td><td>105-7100-060</td><td>Used for AVM embolization</td></tr><tr><td>Angio-Seal Vascular Closure Device</td><td>St. Jude Medical, St Paul, MN</td><td>610130</td><td>Used for femoral artery closure following angiography/intra-arterial embolization</td></tr><tr><td>Midas Rex High Power Drill System</td><td>Medtronic, Minneapolis, MN</td><td>PM700</td><td>Used for craniotomy</td></tr><tr><td>Matchstick Drill Bit</td><td>Medtronic, Minneapolis, MN</td><td>10MH30-MN</td><td>Used to create burr hole for craniotomy</td></tr><tr><td>Tapered Drill Bit</td><td>Medtronic, Minneapolis, MN</td><td>F1/8TA15</td><td>Used to complete craniotomy</td></tr><tr><td>#11 and 15 Blade Surgical Scalpels</td><td>BD Bard-Parker, Franklin Lakes, NJ</td><td>372615</td><td>Used for groin incision for angiography and dural opening for external ventricular drain placement or AVM resection</td></tr><tr><td>Metzenbaum Dissecting Scissors</td><td>Stoelting Co, Wood Dale, IL</td><td>52134-01P</td><td>Used for dural opening</td></tr><tr><td>Bone Elevator</td><td>Stoelting Co, Wood Dale, IL</td><td>52169</td><td>Used for separating dura from the inner skull</td></tr><tr><td>Gerald Forceps</td><td>Stoelting Co, Wood Dale, IL</td><td>52106-52</td><td>Used for dural opening and manipulation</td></tr><tr><td>Microsurgical Instruments</td><td>Accurate Surgical &amp;amp; Scientific Instruments Corporation, Westbury, NY</td><td>ASSI.BML1</td><td>Used for AVM microsurgical resection</td></tr><tr><td>Bipolar Forceps</td><td>Accurate Surgical &amp;amp; Scientific Instruments Corporation, Westbury, NY</td><td>ASSI.BPNS20423FP</td><td>Used for AVM microsurgical resection</td></tr><tr><td>Electrosurgery Generator</td><td>Bovie Medical Products, Clearwater, FL</td><td>IDS-200</td><td>Used for electrosurgical cutting/coagulation</td></tr><tr><td>Small Aneurysm Clips</td><td>Codman Neuro, Raynham, MA</td><td>20-1801</td><td>Used for occlusion of arterial AVM feeders not amenable to coagulation</td></tr><tr><td>Brain Retractors</td><td>Medicon, Tuttlingen, Germany</td><td>22.00.06</td><td>For brain retraction for deep AVM dissection/resection</td></tr><tr><td>Variable Action Suction tip</td><td>Millennium Surgical, Narberth, PA</td><td>6-8607</td><td>For suction with AVM dissection/resection</td></tr><tr><td>Fibrillar Absorbable Hemostatic Agent</td><td>Ethicon, Somerville, NJ</td><td>63713-0019-61</td><td>For hemostatis within surgical cavity</td></tr><tr><td>4-0 Suture</td><td>Ethicon, Somerville, NJ</td><td>C554D</td><td>For dural closure</td></tr><tr><td>2-0 Absorbable Suture</td><td>Ethicon, Somerville, NJ</td><td>J286G</td><td>For deep tissue closure</td></tr><tr><td>3-0 Nylon Suture</td><td>Ethicon, Somerville, NJ</td><td>ET-663G</td><td>For skin closure</td></tr><tr><td>Surgical Staples</td><td>Medline, Mundelein, IL</td><td>STAPLER35RB</td><td>For skin closure</td></tr><tr><td>Bone Plating System</td><td>Biomet, Warsaw, IN</td><td>15-7378-12</td><td>For bone flap securement</td></tr><tr><td>Operating Microscope</td><td>Leica Microsystems, Buffalo Grove, IL</td><td>M720 OH5</td><td>Used for AVM microsurgical resection</td></tr><tr><td>BrainLab Neuronavigation Imaging System</td><td>Brainlab, Inc, Chicago, IL</td><td>Brainlab Curve&amp;nbsp;</td><td>Used for AVM microsurgical resection</td></tr><tr><td>Lumbar External Drainage System</td><td>Codman Neuro, Raynham, MA</td><td>K964923</td><td>Used for placement of lumbar drain for CSF drainage</td></tr><tr><td>External Ventricular Drainage Catheter</td><td>Medtronic, Minneapolis, MN</td><td></td><td>Used for placement of ventricular catheter for CSF drainage</td></tr><tr><td>Disposable Raney Scalp Clips</td><td>A&amp;amp;E Medical Corporation, Farmingdale, NJ</td><td>070-001</td><td>Used for scalp hemostasis</td></tr></tbody></table>

comprehensive endovascular and open surgical management of cerebral arteriovenous malformations

Arteriovenious malformations (AVMs) are associated with significant morbidity and mortality, and have a rupture risk of ~3% per year. Treatment of AVMs must be tailored specifically to the lesion, with surgical resection being the gold standard for small, accessible lesions. Pre-operative embolization of AVMs can reduce nidal blood flow and remove high-risk AVM features such as intranidal or venous aneurysms, thereby simplifying a challenging neurosurgical procedure. Herein, we describe our approach for the staged endovascular embolization and open resection of AVMs, and highlight the advantages of having a comprehensively trained neurovascular surgeon leading a multi-disciplinary clinical team. This includes planning the craniotomy and resection to immediately follow the final embolization stage, thereby using a single session of anesthesia for aggressive embolization, and rapid resection. Finally, we provide a representative case of a 22-year-old female with an unruptured right frontal AVM diagnosed during a seizure workup, who was successfully treated via staged embolizations followed by open surgical resection.

A 22-year-old previously healthy female presented with new onset seizures. Non-contrast head CT was negative for acute hemorrhage, but revealed an incompletely characterized right frontal lesion. MRI demonstrated an approximately 2.9 x 2.4 cm Spetzler-Martin Grade 3 AVM within the right superior frontal gyrus (Figure 1), with large draining cortical veins going to the superior sagittal sinus, and an arterial supply via large branches off the right middle cerebral artery. The patient underwent multiple staged endovascular embolizations, culminating in an embolization of a right anterior cerebral artery pedicle (Figure 2). At the completion of these staged embolizations there was residual supply to the nidus via distal right middle and anterior cerebral artery branches (Figure 3), and indirect supply from the left external carotid artery via distal superior temporal artery branches that anastomosed to the middle meningeal artery via transosseous collaterals.
The patient then underwent a frontotemporal craniotomy by the same comprehensively trained neurovascular surgeon, wherein the medial draining veins were identified early and protected. All arterial feeders were identified, bipolared, and cut to achieve sequential devascularization prior to removal of the AVM nidus. Intra-operative and post-operative catheter angiogram (Figure 4) confirmed complete resection. One month post-operatively the patient was stable neurologically and being weaned from anti-seizure medications, with plans for delayed cerebrovascular imaging at one year.
<img alt="Figure 1" src="/files/ftp_upload/55522/55522fig1.jpg" /> 
Figure 1: Initial imaging of a Spetzler-Martin Grade 3 unruptured right frontal AVM. 
a) Serial axial (i-iii) and b) coronal post-contrast T1-weighted MRI images demonstrating the AVM nidus and medial draining veins. c) Redemonstration of nidus and draining veins on axial T2 Flair MRI imaging. d) Serial AP (i-ii) and lateral (iii-iv) right internal carotid catheter angiogram runs re-demonstrating the AVM nidus and draining veins. <a href="https://cloudflare-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/55522/55522fig1large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 2" src="/files/ftp_upload/55522/55522fig2.jpg" /> 
Figure 2: Catheter angiogram images from final AVM embolization. 
a) Serial oblique views (i-ii) of microcatheter exploration of the distal right anterior cerebral artery (ACA) during establishment of embolization position in the right ACA pedicle exclusively supplying the AVM. (b) Oblique unsubtracted image demonstrating the Onyx cast within the AVM at the conclusion of the final embolization. <a href="https://cloudflare-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/55522/55522fig2large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 3" src="/files/ftp_upload/55522/55522fig3.jpg" /> 
Figure 3: Catheter angiogram post final staged embolization demonstrating residual AVM nidal filling. 
a) Serial oblique views of a right internal carotid injection (i-vi) following Onyx embolization of a right anterior cerebral artery pedicle via the left internal carotid and anterior communicating artery. b) Serial AP views of a left internal carotid injection following the above embolization (i-ii). Residual supply to the nidus is seen from distal right middle cerebral artery branches, and distal right anterior cerebral artery branches filling from both the left and right internal carotids. <a href="https://cloudflare-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/55522/55522fig3large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 4" src="/files/ftp_upload/55522/55522fig4.jpg" /> 
Figure 4: Post-operative catheter angiogram demonstrating complete AVM resection. 
Serial oblique views of a right internal carotid injection (i-v) on post-operative day 1 demonstrating complete AVM resection. <a href="https://cloudflare-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/55522/55522fig4large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>

Watch this Scientific Journal Video about Comprehensive Endovascular and Open Surgical Management of Cerebral Arteriovenous Malformations at JoVE.com

Comprehensive Endovascular and Open Surgical Management of Cerebral Arteriovenous Malformations

Surgery is the gold standard for accessible arteriovenious malformations (AVMs), and pre-operative embolization can simplify this procedure. We describe our approach for staged endovascular embolization and open resection of AVMs, and provide a representative clinical example highlighting the advantages of a comprehensively trained neurovascular surgeon leading a multi-disciplinary clinical team.

Arteriovenious malformations (AVMs) are associated with significant morbidity and mortality, and have a rupture risk of ~3% per year. Treatment of AVMs ...

comprehensive-endovascular-open-surgical-management-cerebral

Nanyang Technological University

Research

JoVE Journal

Neuroscience

9.5K Views.  University of California, San Diego. Surgery is the gold standard for accessible arteriovenious malformations (AVMs), and pre-operative embolization can simplify this procedure. We describe our approach for staged endovascular embolization and open resection of AVMs, and provide a representative clinical example highlighting the advantages of a comprehensively trained neurovascular surgeon leading a multi-disciplinary clinical team.

Video: Comprehensive Endovascular and Open Surgical Management of Cerebral Arteriovenous Malformations

Microsurgical Venous Pouch Arterial-Bifurcation Aneurysms in the Rabbit Model: Technical Aspects

For ruptured human cerebral aneurysms endovascular embolization has become an equivalent alternative to aneurysm clipping.1 However, large clinical trials have shown disappointing long-term results with unacceptable high rates of aneurysm recanalization and delayed aneurysm rupture.2 To overcome these problems, animal experimental studies are crucial for the development of better endovascular devices.3-5
Several animal models in rats, rabbits, canines and swine are available.6-8 Comparisons of the different animal models showed the superiority of the rabbit model with regard to hemodynamics and comparability of the coagulation system and cost-effectiveness.9-11 
The venous pouch arterial bifurcation model in rabbits is formed by a venous pouch sutured into an artificially created true bifurcation of both common carotid arteries (CCA). The main advantage of this model are true bifurcational hemodynamics.12 The major drawbacks are the sofar high microsurgical technical demands and high morbidity and mortality rates of up to 50%.13 These limitations have resulted in less frequent use of this aneurysm model in the recent years. These shortcomings could be overcome with improved surgical procedures and modified peri- and postoperative analgetic management and anticoagulation.14-16 Our techniques reported in this paper demonstrate this optimized technique for microsurgical creation of arterial bifurcation aneurysms.

An optimized technique for the microsurgical creation of arterial bifurcation aneurysms mimicking bifurcation human cerebral aneurysms is described. A venous pouch is sutured into an artificially created true bifurcation of both common carotid arteries. Facilitated microsurgical techniques and aggressive postoperative anticoagulation and analgesia lead to minimized morbidity rates and high aneurysm patency rates.

For ruptured human cerebral aneurysms endovascular embolization has become an equivalent alternative to aneurysm clipping.1 However, large clinical trials ...

Medicine

Permanent Cerebral Vessel Occlusion via Double Ligature and Transection

Stroke is a leading cause of death, disability, and socioeconomic loss worldwide. The majority of all strokes result from an interruption in blood flow (ischemia) 1. Middle cerebral artery (MCA) delivers a great majority of blood to the lateral surface of the cortex 2, is the most common site of human stroke 3, and ischemia within its territory can result in extensive dysfunction or death 1,4,5. Survivors of ischemic stroke often suffer loss or disruption of motor capabilities, sensory deficits, and infarct. In an effort to capture these key characteristics of stroke, and thereby develop effective treatment, a great deal of emphasis is placed upon animal models of ischemia in MCA.
Here we present a method of permanently occluding a cortical surface blood vessel. We will present this method using an example of a relevant vessel occlusion that models the most common type, location, and outcome of human stroke, permanent middle cerebral artery occlusion (pMCAO). In this model, we surgically expose MCA in the adult rat and subsequently occlude via double ligature and transection of the vessel. This pMCAO blocks the proximal cortical branch of MCA, causing ischemia in all of MCA cortical territory, a large portion of the cortex. This method of occlusion can also be used to occlude more distal portions of cortical vessels in order to achieve more focal ischemia targeting a smaller region of cortex. The primary disadvantages of pMCAO are that the surgical procedure is somewhat invasive as a small craniotomy is required to access MCA, though this results in minimal tissue damage. The primary advantages of this model, however, are: the site of occlusion is well defined, the degree of blood flow reduction is consistent, functional and neurological impairment occurs rapidly, infarct size is consistent, and the high rate of survival allows for long-term chronic assessment.

Permanent Cerebral Vessel Occlusion via Double Ligature and Transection

We describe a highly reproducible method for the permanent occlusion of a rodent major cerebral blood vessel. This technique can be accomplished with very little peripheral damage, minimal blood loss, a high rate of long-term survival, and consistent infarct volume commensurate with the human clinical population.

Stroke is a leading cause of death, disability, and socioeconomic loss worldwide. The majority of all strokes result from an interruption in blood flow ...

Adult Mouse Venous Hypertension Model: Common Carotid Artery to External Jugular Vein Anastomosis.

The understanding of the pathophysiology of brain arteriovenous malformations and arteriovenous fistulas has improved thanks to animal models. A rat model creating an artificial fistula between the common carotid artery (CCA) and the external jugular vein (EJV) has been widely described and proved technically feasible. This construct provokes a consistent cerebral venous hypertension (CVH), and therefore has helped studying the contribution of venous hypertension to formation, clinical symptoms, and prognosis of brain AVMs and dural AVFs. Equivalent mice models have been only scarcely described and have shown trouble with stenosis of the fistula. An established murine model would allow the study of not only pathophysiology but also potential genetic therapies for these cerebrovascular diseases.
We present a model of arteriovenous fistula that produces a durable intracranial venous hypertension in the mouse. Microsurgical anastomosis of the murine CCA and EJV can be difficult due to diminutive anatomy and frequently result in a non-patent fistula. In this step-by-step protocol we address all the important challenges encountered during this procedure. Avoiding excessive retraction of the vein during the exposure, using 11-0 sutures instead of 10-0, and making a carefully planned end-to-side anastomosis are some of the critical steps. Although this method requires advanced microsurgical skills and a longer learning curve that the equivalent in the rat, it can be consistently developed.
This novel model has been designed to integrate transgenic mouse techniques with a previously well-established experimental system that has proved useful to study brain AVMs and dural AVFs. By opening the possibility of using transgenic mice, a broader spectrum of valid models can be achieved and genetic treatments can also be tested. The experimental construct could also be further adapted to the study of other cerebrovascular diseases related with venous hypertension such as migraine, transient global amnesia, transient monocular blindness, etc.

We describe a method for creating a reliable model of cerebral venous hypertension in the adult mouse. This model has been widely described and tested in the rat. This new counterpart in the mice opens the possibility of using genetic modified animals and thereby broadens the applications of the model.

The understanding of the pathophysiology of brain arteriovenous malformations and arteriovenous fistulas has improved thanks to animal models. A rat model ...

Microsurgical Clip Obliteration of Middle Cerebral Aneurysm Using Intraoperative Flow Assessment

Cerebral aneurysms are abnormal widening or ballooning of a localized segment of an intracranial blood vessel.  Surgical clipping is an important treatment for aneurysms which attempts to exclude blood from flowing into the aneurysmal segment of the vessel while preserving blood flow in a normal fashion.  Improper clip placement may result in residual aneurysm with the potential for subsequent aneurysm rupture or partial or full occlusion of distal arteries resulting in cerebral infarction.  Here we describe the use of an ultrasonic flow probe to provide quantitative evaluation of arterial flow before and after microsurgical clip placement at the base of a middle cerebral artery aneurysm.  This information helps ensure adequate aneurysm reconstruction with preservation of normal distal blood flow.

Description of the surgical obliteration of a cerebral aneurysm utilizing an ultrasonic flow probe to assess arterial flow prior to and after aneurysm clip placement.

Cerebral aneurysms are abnormal widening or ballooning of a localized segment of an intracranial blood vessel.  Surgical clipping is an important ...

Biology

Minimally Invasive Thumb-sized Pterional Craniotomy for Surgical Clip Ligation of Unruptured Anterior Circulation Aneurysms

Less invasive surgical approaches for intracranial aneurysm clipping may reduce length of hospital stay, surgical morbidity, treatment cost, and improve patient outcomes. We present our experience with a minimally invasive pterional approach for anterior circulation aneurysms performed in a major tertiary cerebrovascular center and compare the results with an aged matched dataset from the Nationwide Inpatient Sample (NIS). From August 2008 to December 2012, 22 elective aneurysm clippings on patients &#8804;55 years of age were performed by the same dual fellowship-trained cerebrovascular/endovascular neurosurgeon. One patient (4.5%) experienced transient post-operative complications. 18 of 22 patients returned for follow-up imaging and there were no recurrences through an average duration of 22 months. A search in the NIS database from 2008 to 2010, also for patients aged &#8804;55 years of age, yielded 1,341 hospitalizations for surgical clip ligation of unruptured cerebral aneurysms. Inpatient length of stay and hospital charges at our institution using the minimally invasive thumb-sized pterional technique were nearly half that of NIS (length of stay: 3.2 vs 5.7 days; hospital charges: $52,779 vs. $101,882). The minimally invasive thumb-sized pterional craniotomy allows good exposure of unruptured small and medium-sized supraclinoid anterior circulation aneurysms. Cerebrospinal fluid drainage from key subarachnoid cisterns and constant bimanual microsurgical techniques avoid the need for retractors which can cause contusions, localized venous infarctions, and post-operative cerebral edema at the retractor sites. Utilizing this set of techniques has afforded our patients with a shorter hospital stay at a lower cost compared to the national average.

Minimally invasive thumb-sized pterional craniotomy for aneurysm clipping has afforded our patients with a shorter hospital stay at a lower cost compared to the national average.

Less invasive surgical approaches for intracranial aneurysm clipping may reduce length of hospital stay, surgical morbidity, treatment cost, and improve ...

Isolation and Cannulation of Cerebral Parenchymal Arterioles

Intracerebral parenchymal arterioles (PAs), which include parenchymal arterioles, penetrating arterioles and pre-capillary arterioles, are high resistance blood vessels branching out from pial arteries and arterioles and diving into the brain parenchyma. Individual PA perfuse a discrete cylindrical territory of the parenchyma and the neurons contained within. These arterioles are a central player in the regulation of cerebral blood flow both globally (cerebrovascular autoregulation) and locally (functional hyperemia). PAs are part of the neurovascular unit, a structure that matches regional blood flow to metabolic activity within the brain and also includes neurons, interneurons, and astrocytes. Perfusion through PAs is directly linked to the activity of neurons in that particular territory and increases in neuronal metabolism lead to an augmentation in local perfusion caused by dilation of the feed PA. Regulation of PAs differs from that of better-characterized pial arteries. Pressure-induced vasoconstriction is greater in PAs and vasodilatory mechanisms vary. In addition, PAs do not receive extrinsic innervation from perivascular nerves &#8212; innervation is intrinsic and indirect in nature through contact with astrocytic endfeet. Thus, data regarding contractile regulation accumulated by studies using pial arteries does not directly translate to understanding PA function. Further, it remains undetermined how pathological states, such as hypertension and diabetes, affect PA structure and reactivity. This knowledge gap is in part a consequence of the technical difficulties pertaining to PA isolation and cannulation. In this manuscript we present a protocol for isolation and cannulation of rodent PAs. Further, we show examples of experiments that can be performed with these arterioles, including agonist-induced constriction and myogenic reactivity. Although the focus of this manuscript is on PA cannulation and pressure myography, isolated PAs can also be used for biochemical, biophysical, molecular, and imaging studies.

This manuscript describes a simple and reproducible protocol for isolation of intracerebral arterioles (a group of blood vessels encompassing parenchymal arterioles, penetrating arterioles and pre-capillary arterioles) from mice, to be used in pressure myography, immunofluorescence, biochemistry, and molecular studies.

Intracerebral parenchymal arterioles (PAs), which include parenchymal arterioles, penetrating arterioles and pre-capillary arterioles, are high resistance ...

Surgical Approach for Middle Cerebral Artery Occlusion and Reperfusion Induced Stroke in Mice

Stroke is a leading cause of death worldwide and continues to be one of the major causes of long-term adult disabilities. About 87% of strokes are ischemic in origin and occur in the territory of the middle cerebral artery (MCA). Currently the only Food and Drug Administration (FDA) approved drug for the treatment of this devastating disease is tissue plasminogen activator (tPA). However, tPA has a small therapeutic window for administration (3 - 6 hr), and is only effective in 4% of the patients who actually receive it. Current research focuses on understanding the pathophysiology of stroke in order to find potential therapeutic targets. Thus, reliable models are crucial, and the MCA occlusion (MCAo) model (also termed the intraluminal filament or suture model) is deemed to be the most clinically relevant surgical model of ischemic stroke, and is fairly non-invasive and easily reproducible. Typically the MCAo model is used with rodents, especially with mice due to all the genetic variations available for this species. Here we describe (and present in the video) how to successfully perform the MCAo model (with reperfusion) in mice to generate reliable and reproducible data.

In order to understand the pathophysiology of stroke, it is important to use reliable models. This paper will describe one of the most frequently used stroke models in mice, termed the middle cerebral artery occlusion (MCAo) model (also termed the intraluminal filament or suture model) with reperfusion.

Stroke is a leading cause of death worldwide and continues to be one of the major causes of long-term adult disabilities. About 87% of strokes are ...

Simulator Training for Endovascular Neurosurgery

Simulation-based training has become common practice across medical specialties, especially for learning complex skills performed in high-risk environments. In the field of endovascular neurosurgery, the demand for consequence- and risk-free learning environments led to the development of simulation devices valuable for medical trainees. The goal of this protocol is to provide instructive guidelines for the use of an endovascular neurosurgery simulator in an academic setting. The simulator provides trainees with the opportunity to receive realistic feedback on their knowledge of anatomy, as well as haptic feedback indicative of their success in handling the catheter-based systems without negative consequences. The utility of this specific protocol in relation to other neuroendovascular training modalities is also discussed.

Simulation of complex, high-risk procedures is critical to the education of medical trainees. A protocol for simulator-based endovascular neurosurgery training in a controlled academic environment is described. The protocol includes stepwise guidelines for trainees of varying levels, with a discussion of the advantages and limitations of this model.

Simulation-based training has become common practice across medical specialties, especially for learning complex skills performed in high-risk ...

Transvenous Embolization of Carotid Cavernous Fistula through Inferior Petrosal Sinus with Detachable Coils and Ethylene Vinyl Alcohol Copolymer

Carotid cavernous fistula (CCF) is a rare disease caused by abnormal communications between the internal carotid artery (direct fistula) or meningeal branches of the external carotid artery (indirect fistula) and the cavernous sinus (CS). Trauma is the most common cause of CCF. The clinical presentation of CCF is closely related to the venous drainage pattern. Orbital and neuro-ophthalmological symptoms are the most common clinical presentation of CCF with drainage through the superior ophthalmic vein (SOV). Endovascular embolization by arterial or venous approaches is the most common management of CCF. Transvenous embolization using detachable coils and ethylene-vinyl alcohol copolymer (EVOH) is an alternative method for the treatment of CCF. Endovascular embolization offers different options to treat CCF by minimally invasive approach decreasing morbidity and residual fistulas. The purpose of this article is to report our treatment experiences via the inferior petrosal sinus (IPS), and immediate-term outcomes of endovascular embolization of CCF by using detachable coils and EVOH.

The purpose of the article is to present our experience in endovascular treatment via the inferior petrosal sinus of the carotid cavernous fistula with detachable coils and ethylene-vinyl alcohol copolymer.

Carotid cavernous fistula (CCF) is a rare disease caused by abnormal communications between the internal carotid artery (direct fistula) or meningeal ...

Neuronavigation and Laparoscopy Guided Ventriculoperitoneal Shunt Insertion for the Treatment of Hydrocephalus

Hydrocephalus is a common adult neurosurgical condition typically requiring treatment with a cerebrospinal fluid (CSF) shunt, of which the ventriculoperitoneal (VP) shunt is the most common type. Unfortunately, the failure rates of VP shunts are alarmingly high, with up to 50% of patients requiring revision surgery within 2 years. VP shunt failure may occur due to infection, or catheter mispositioning, migration, and occlusion. We undertook a joint neurosurgery and general surgery collaboration in a 7-year prospective non-randomized consecutive quality improvement cohort study to reduce the rates of ventriculoperitoneal (VP) shunt failures in 224 adult patients at a tertiary care institution. The initiative combined the use of electromagnetic stereotactic neuronavigation to guide the placement of the proximal catheter and laparoscopy to place the distal catheter under direct visualization. With laparoscopic assistance, the distal catheter was anchored through a small hole created in the falciform ligament and placed into the right retrohepatic space, free from the omentum, adhesions, or bowel that might obstruct the catheter tip. The surgeries were performed using a shunt infection prevention protocol to reduce the risk of shunt infections. Here, we present an intraoperative video of the surgical procedure. Compliance with shunt infection reduction strategies and the combined utilization of neuronavigation and laparoscopy techniques in adult VP shunt surgery resulted in a 44% reduction in the risk of overall shunt failure. The significant positive impact with regard to shunt-failure-free patient outcomes among patients who underwent VP shunt surgery using this strategy underscores the value associated with the use of these modern intraoperative techniques and cross-specialty collaboration during VP shunt surgery.

Patient outcomes of ventriculoperitoneal (VP) shunt surgery, the mainstay treatment for hydrocephalus in adults, are poor due to high shunt failure rates. We present intraoperative footage of VP shunt insertion using neuronavigation and laparoscopy guidance, with the goal to reduce the risks of proximal and distal shunt catheter failures, respectively.

Comprehensive Endovascular and Open Surgical Management of Cerebral Arteriovenous Malformations

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Rozdziały w tym wideo

Microsurgical Venous Pouch Arterial-Bifurcation Aneurysms in the Rabbit Model: Technical Aspects

Permanent Cerebral Vessel Occlusion via Double Ligature and Transection

Adult Mouse Venous Hypertension Model: Common Carotid Artery to External Jugular Vein Anastomosis.

Microsurgical Clip Obliteration of Middle Cerebral Aneurysm Using Intraoperative Flow Assessment

Minimally Invasive Thumb-sized Pterional Craniotomy for Surgical Clip Ligation of Unruptured Anterior Circulation Aneurysms

Isolation and Cannulation of Cerebral Parenchymal Arterioles

Surgical Approach for Middle Cerebral Artery Occlusion and Reperfusion Induced Stroke in Mice

Simulator Training for Endovascular Neurosurgery

Transvenous Embolization of Carotid Cavernous Fistula through Inferior Petrosal Sinus with Detachable Coils and Ethylene Vinyl Alcohol Copolymer

Neuronavigation and Laparoscopy Guided Ventriculoperitoneal Shunt Insertion for the Treatment of Hydrocephalus