Comprehensive Endovascular and Open Surgical Management of Cerebral Arteriovenous Malformations

Summary

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.

Abstract

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.

Introduction

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 scales^1,8 as well as surgeon and multidisciplinary conference evaluations) at our institution.

Protocol

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.

1. 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
2. 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.
3. If the patient is neurologically stable, obtain informed consent and book the patient for definitive vascular imaging via six-vessel catheter angiography ± 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 ± AVM resection (see section 4 below) prior to or immediately following diagnostic six-vessel catheter angiography.

2. Six-vessel angiography

1. 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
2. Place a right femoral artery sheath using a micropuncture groin access kit and a modified Seldinger technique.¹²
   1. Clean (with 2% chlorhexidine gluconate and 70% isopropyl alcohol) and sterilely drape the groin.
   2. 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° angle to the skin.
   3. 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.
   4. 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.
   5. Insert a J-wire through the lumen of the vessel dilator, and remove the vessel dilator, keeping the J-wire in place.
   6. 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.
3. 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.
4. Review recorded angiographic images of the above vessel runs to determine the feeding vessels and draining veins of the AVM.
5. 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.

3. AVM embolization

NOTE: If the AVM is amenable to endovascular and subsequent surgical treatment (as defined by established grading scales^1,8 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.

1. 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).
2. 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
3. Obtain femoral arterial access utilizing the modified Seldinger technique and insert a 6- French femoral sheath as in 2.2.
4. 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.
5. 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) 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.
6. 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.
7. 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.
8. 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 <40% of the nidus are embolized in a single procedure, making staged embolizations common.
9. 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.
10. 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).

4. AVM resection

1. 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.
2. In conjunction with a neuromonitoring team, establish baseline neuromonitoring as described in 3.2, with continued monitoring throughout the case.
3. Sync pre-operative imaging with intra-operative neuro-navigation system using surface matching, marker, or pointer registration as per neuronavigation system specifications.
4. Obtain groin access as in step 2.2, if sheath is not already in place.
5. Perform a craniotomy tailored to the specific AVM location within the cranium using a high-power drill system, ensuring a wide bony exposure.
   1. 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.  Irrigate and obtain hemostasis.
   2. 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.
   3. 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.
   4. Alternatively, place an external ventricular drain into the lateral ventricle at either Frazier's or Kocher'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.
6. 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.
7. 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.
   1. 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.
   2. 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.
   3. 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.
   4. 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.
   5. 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.
   6. 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.
8. 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.
9. 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.
10. Extubate if able, and transfer the patient to the ICU for close neurologic monitoring and recovery.

5. Long term follow up

1. 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.

Results

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. ...

Discussion

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, th...

Materials

List of materials used in this article

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