Neuroimaging: Interventional Neuroradiology: Neurological Endovascular Therapy in Hemorrhagic and Ischemic Strokes

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Chapter 33E Neuroimaging

Interventional Neuroradiology: Neurological Endovascular Therapy in Hemorrhagic and Ischemic Strokes

Historical Background

Neurological endovascular therapy is a relatively new subspecialty dealing with a wide range of pathologies linked to central nervous system (CNS) hemorrhagic (Jabbour et al., 2009; Pearl et al., 2010) or ischemic (Santos-Franco et al., 2009; Thorisson and Johnson, 2009; Zenteno-Castellanos et al., 2009) disorders of arteries and veins (Caso et al., 2008) and of the head and neck (Gandhi et al., 2008; Sekhar et al., 2009; Turowski and Zanella, 2003). Working closely with different disciplines—stroke neurology, diagnostic and interventional neuroradiology, neurosurgery, neurointensive care, and neurorehabilitation (Connors et al., 2005; Qureshi et al., 2008)—endovascular therapy plays a key role in patient management.

Endovascular therapy has evolved in the last 25 years. Thanks to rapid technological developments, better knowledge of applied neuroanatomy, and greater understanding of the pathological processes, many procedures that were previously risky and often ineffective now produce excellent clinical results with low morbidity and mortality (Naggara et al., 2010). The implementation of neurointerventional procedures requires a multidisciplinary team including neuroanesthesiologists (Brekenfeld et al., 2010; Varma et al., 2007; Young, 2007), neurosurgeons, radiologists, critical care specialists (Bruder et al., 2008; Connolly et al., 2005), and neurologists, along with a well-trained staff of nurses (Galimany-Masclans et al., 2009; Wright, 2007) and technologists. Additionally, some studies comparing the length of stay and total hospital charges have recently favored interventional treatment over surgical procedures in selected cases (Hoh et al., 2010).

Since the first in vivo angiography performed by Edgas Moniz in 1927, this technique has evolved significantly from direct puncture of cervical vessels to transfemoral or transradial approaches to the neurovascular structures (Jo et al., 2010). In the late 1970s, most of the procedures were limited to the extracranial vasculature. In 1976, Kerber described a balloon catheter with a calibrated leak as a new system for super-selective angiography and occlusive catheter therapy. Flow-guided catheters were soon replaced by more soft, trackable devices. The use of latex/silicone detachable balloons and mechanically driven coils were also soon complemented by the addition of particles, liquid embolic agents, and electrically detachable coils.

The diagnostic and technical excellence brought by digital subtraction angiography was also improved with the development of new guide wires and hydrophilic microcatheters. New angiography techniques were incorporated, such as high-speed serial imaging, road mapping (Rossitti and Pfister, 2009), contrast injectors, and the availability of biplanar rotational (Dorfler et al., 2008) three-dimensional (3D) flat-panel angiography and C-arm flat-detector computed tomography (CT) (Kamran et al., 2010). Noninvasive imaging techniques such as computed tomography angiography (CTA) and magnetic resonance angiography (MRA) complement the use of digital 3D subtraction angiography, though the latter remains the diagnostic gold standard owing to its more accurate assessment of intracranial and spinal vascular anatomical and dynamic information (Mo et al., 2010). Interventional neuroradiology is a discipline that brings together three major branches of the neurosciences: observation through neuroradiology, technical mastery of neurosurgery, and clinical skills of neurology. Combining these three skill sets allows endovascular therapy to be both comprehensive and effective in the diagnosis and management of patients with vascular disorders of the CNS.

Intracranial Vascular Malformations

Brain Arteriovenous Malformations

As seen in Table 33E.1, arteriovenous malformations (AVMs) can be divided into two different groups (Chaloupka and Huddle, 1998). The group in the left column is suitable for neurointerventional management.

Table 33E.1 Types of Arteriovenous Malformations with and without Shunts

Present Absent
Arteriovenous malformation Capillary vessel malformations (telangiectasias)
Pial arteriovenous fistulas Developmental venous anomalies (venous angiomas)
Dural arteriovenous fistulas Cavernous angiomas

Epidemiology and Pathology

Brain AVMs are the more frequent type of vascular malformations and those which cause the most morbidity and mortality. The true incidence is difficult to estimate, but some retrospective population-based studies have shown that the incidence of symptomatic intracranial hemorrhage (ICH) due to any type of intracranial vascular malformations was 0.8 per 100,000 (Brown et al., 1996a). The New York Island Arteriovenous Malformation Study was the first ongoing prospective population-based survey to determine the incidence of AVM hemorrhage and associated morbidity and mortality rates in New York City. Initial results calculated an AVM detection rate of 1.34 per 100,000 person-years and an acute AVM hemorrhage rate of 0.51 per 100,000 person-years (Stapf et al., 2003).

Some 90% of brain AVMs are supratentorial, and 10% are infratentorial. An AVM is a complex tangled bundle of abnormal arteries and veins linked by one or more fistulas (Choi and Mohr, 2005). An important anatomical feature of this vascular conglomerate, also known as a nidus, is the lack of a capillary bed (Choi and Mohr, 2005). The nidus is surrounded by gliotic tissue with traces of hemosiderin and calcifications due to previous bleeds. Most AVMs harbor intracranial aneurysms, which can be intranidal, related to the AVM (distal or proximal arising from the feeder vessels), or located in different parts of the arterial circulation.

Natural History

The clinical presentation generally occurs between the second and fourth decades of life. The natural history of unruptured AVMs is unclear. A Randomized Trial of Unruptured Brain Arteriovenous Malformations (ARUBA) is underway to address this issue (Stapf et al., 2006). About 50% of patients harboring a brain AVM present with hemorrhage (intraparenchymal, subarachnoid, or intraventricular) (Brown et al., 1996b). In the Cooperative Study of Intracranial Aneurysms and Subarachnoid Hemorrhage, symptomatic AVMs were found in 8.6% of all patients with nontraumatic subarachnoid hemorrhages. Seizures are the second most common presentation, followed by headache and progressive focal neurological deficit. The risk of hemorrhage is 1.3% to 3.9% yearly after diagnosis of an AVM in patients who present without ICH. For patients with a previous hemorrhage, the risk of rebleeding is between 6% and 17% in the first year (Fleetwood and Steinberg, 2002), diminishing thereafter.

Various angiographic and clinical factors predictive of bleeding have been identified in retrospective studies and include (Fleetwood and Steinberg, 2002): previous hemorrhage, deep venous drainage, unique venous drainage, venous stenosis or aneurysms, intranidal aneurysms, venous reflux into a venous sinus, small nidus size, high-feeding artery pressure, slow arterial filling, and deep/periventricular location.

Imaging and Classification

Several imaging findings in brain AVMs influence the patient’s therapeutic and clinical management decisions. The most important ones are those known to be associated with hemorrhage or risk of future hemorrhage (evidence of previous hemorrhage, intranidal aneurysms, venous stenosis, deep venous drainage, and deep location of the nidus) (Geibprasert et al., 2010). Magnetic resonance imaging (MRI) is more sensitive than CT in the diagnosis of an AVM and is useful in accurately identifying its location and relationship to functional regions. The most significant features are flow-void signal and hemosiderin deposits in T1- and T2-weighted images. Functional MRI plays an important role in interventional management because it facilitates the localization of functionally important brain areas adjacent to the AVM nidus (Schlosser et al., 1997). Although MRA provides useful information on AVM feeder arteries and draining veins, digital 3D cerebral angiography is the gold standard (Strozyk et al., 2009) for the acquisition of accurate anatomical and dynamic information. The addition of superselective catheterization and angiography of AVM arterial feeders adds key information on AVM angioarchitecture (identification of high-flow arteriovenous fistulas [AVFs], intranidal aneurysms, and selective stenosis of AVM-draining veins).

AVMs can be superficial (sulcal/gyral) or deep (deep parenchymal/choroid plexus). In the sulcal type, the nidus is located in the subpial space and has a conical or wedge-shaped morphology. In the gyral type, AVMs tend to be spherical, since they are covered with cortex. These AVMs have feeding arteries that continue beyond the lesion to supply healthy brain tissue (arteries “en passage”) (Choi and Mohr, 2005).

Mixed malformations are larger and have sulcal and gyral features. The location of the AVM nidus is important because it can predict its pattern of venous drainage. Cortical AVMs typically drain through cortical veins into a dural sinus. When they have a subcortical or ventricular extension, they have superficial and deep venous drainage. Angiography should provide information on: (1) the nidus (single or multiple compartments, plexiform, fistulous), (2) the number and origin of feeding arteries (pial, dural, leptomeningeal, choroidal, or perforating), (3) type of venous drainage, and (4) presence of intranidal aneurysms.

Morphological characteristics (size and location) and drainage patterns of the AVM are used to classify patients for the risk of persistent neurological deficits from surgery (Choi and Mohr, 2005).

The classification used in clinical practice for surgical management is the Spetzler-Martin grading scale based on three criteria: (1) size of the AVM, (2) venous drainage, and (3) location (eloquent parenchyma corresponds to sensorimotor cortex, areas of language, visual cortex, hypothalamus, thalamus, internal capsule, brainstem, cerebellar peduncles, and deep cerebellar nuclei). However, one of the original authors has redesigned the grading system into a three-tiered classification of cerebral AVMs (class A combines grades I and II, class B are grade III, and class C combines grades IV and V), offering simplification of the previous placement of patients into five categories, which is intended to provide a guide to treatment and be predictive of outcome (Spetzler and Ponce, 2010). Spetzler-Martin grades were specifically designed to classify surgical patients and do not apply when the patient is managed endovascularly. Risk assessment and outcome determination in brain AVM patients treated by endovascular techniques seem adequate and clinically feasible using other scales (Feliciano et al., 2010).


Multimodality treatment is the best approach in patients with complex AVMs (Yuki et al., 2010). The present therapeutic approaches include radiosurgery (with latency to obliteration of 1 to 3 years) (Yen et al., 2010), surgery (Rubin et al., 2010), and embolization (Valle et al., 2008; Vinuela et al., 2005; Xu et al., 2010). Medium and large AVMs (Valle et al., 2008) or AVMs with large AVFs or intranidal aneurysms also require a multidisciplinary strategy. The endovascular occlusion of large AVFs or intranidal aneurysms associated with an AVM nidus decreases endovascular or surgical complications, mostly related to local and regional high venous pressure and intraoperative bleeding.

Embolization focuses on occlusion of surgically difficult-to-reach arteries (deep arteries), intranidal aneurysms, and AVFs (Yuki et al., 2010). A 48- to 72-hour interval is advised between AVM embolization and final surgical removal. If embolization is performed before radiosurgery (Shtraus et al., 2010), its primary goal is to reduce the size of the AVM, close fistulas, and treat intranidal aneurysms (see Fig. 33E.2). If an AVM is small and has few afferent pedicles, endovascular treatment can be complete and permanent (Oran et al., 2005) (Fig. 33E.1). Embolic materials include:

image Polyvinyl alcohol particles (PVAs): ranging from 14 to 1000 µm. PVAs cause a foreign body inflammatory reaction. Disadvantages are their adhesivity to the microcatheter and high recanalization rates (Sorimachi et al., 1999).

image N-2-butyl-cyanoacrylate (NBCA) (Starke et al., 2009; Yu et al., 2004) causes an inflammatory reaction in arteries and surrounding tissue, leading to necrosis/fibrosis of the vessel. NBCA polymerizes in contact with ionic solutions. An iodized oil-based contrast agent (Lipiodol) is added to the NBCA to control its polymerization rate as well as to opacify the mixture for angiographic visualization (Calvo et al., 2001). The microcatheter must be flushed with 10% dextrose to prevent NBCA polymerization within it. Occlusion of cerebral AVMs with NBCA is generally permanent (Wikholm, 1995). It is essential to deliver the acrylic into the AVM nidus and not in the parent artery alone. Proximal arterial occlusion elicits early AVM recanalization by local collateral circulation, making the postembolization surgical AVM resection more difficult.

image Onyx (Hauck et al., 2009; Xu et al., 2010) is a copolymer of ethylene vinyl alcohol (EVOH) solved in dimethyl sulfoxide (DMSO). When the compound comes in contact with a liquid, it precipitates and forms a sponge-like material. The precipitation progresses centripetally, and the center remains fluid and continues its anterograde flow. Use of Onyx requires DMSO-compatible microcatheters, which are stiffer and often require guide wires for navigation (Weber et al., 2007). The injection of Onyx is slower and more controllable than the NBCA injection. In experienced hands, the percentage of complete AVM occlusion with Onyx reaches 50% (Maimon et al., 2010). NBCA is preferred in fistulous arteriovenous shunts, perforating arteries, leptomeningeal collaterals, and catheter positions distal from the nidus.

image Microcoils are used to occlude high-flow AVFs in combination with AVM nidus. Their main role is to decrease untoward embolization of liquid embolic agents into the AVM venous drainage, dural venous sinus, and pulmonary circulation.

Dural Arteriovenous Fistulas

Dural arteriovenous fistulas (DAVFs) are characterized by discrete AVFs involving the intracranial meninges covering the venous sinuses. Although their etiology remains unknown, in most cases there is evidence that the fistula formation is preceded in some instances by trauma resulting in skull fracture, sinus thromboses, or venous outlet stenoses (Berenstein et al., 2004). They are often located in the cavernous sinus, transverse sigmoid sinus, superior sagittal sinus, foramen ovale, tentorium, and anterior or middle cranial fossae.

The clinical features associated with DAVFs depend on location of the lesion, extent of AV shunting, and associated recruitment pial veins. Symptoms may be benign (asymptomatic, tinnitus, ocular symptoms, cranial nerve palsies) or serious (ICH, focal neurological deficits, dementia, papilledema, and even death). These symptoms are associated with cortical venous reflux and/or development of intracranial hypertension. The risk of bleeding is 2% per year and depends on location and hemodynamics. Bleeding is always of venous origin. Several classifications have been proposed and compared (Davies et al., 1996). The most widely accepted ones are from Cognard et al. (1995) and Borden et al. (1995).

Therapeutic Approach to Cavernous Dural Arteriovenous Fistulas

Intermittent manual compression of the carotid artery may be effective in occluding the cavernous sinus. The ipsilateral carotid artery is compressed using the contralateral hand for approximately 5 minutes every waking hour for 1 to 3 days. If this is tolerated, the compression time is increased to 10 to 15 minutes of compression per waking hour. The compression produces concomitant partial obstruction of the ipsilateral carotid artery and jugular vein. This results in the transient reduction of arteriovenous shunting by decreasing arterial flow while simultaneously increasing the outlet venous pressure, thereby promoting spontaneous thrombosis within the cavernous sinus (Katsaridis, 2009).

Treatment of DAVF may be endovascular (Kathleen et al., 2009; Katsaridis, 2009), radio-surgical, or surgical. The endovascular approach can be performed with detachable coils, cyanoacrylate, or Onyx (Cognard et al., 2008; Jiang et al., 2010) or via the venous route, packing the sinus with coils or Onyx (Lv et al., 2009) (Fig. 33E.2). The objective of the arterial approach is to close the fistula at the origin of the main draining vein. Occlusion of a meningeal fistula proximal to its draining vein elicits rapid development of arterial collaterals and fistula recanalization (“medusa head” angiographic appearance).

Carotid-Cavernous Fistulas

Carotid-cavernous DAVF should be differentiated from direct AVFs involving the cavernous sinus. A well-accepted classification divides them into:

Symptoms and signs tend to be mild, and parenchymal hemorrhage is rare. Orbital pain, proptosis, chemosis, ophthalmoplegia, pulsating noise, increased intraocular pressure, and decrease in visual acuity are usually seen (Jabbour et al., 2009; Zenteno et al., 2010). The treatment of a CCF depends on the severity of clinical symptoms, its angiographic characteristics, and the risk it presents for ICH. In most instances, endovascular treatment is preferred.

Treatment of the CCF can be:

image Intraarterial: detachable balloons (latex/silicone) (Teng et al., 2000), platinum coils, or stent-assisted coiling (Moron et al., 2005). Self-expandable covered stents look very promising but are still under investigation (Gomez et al., 2007). Cyanoacrylate embolization has a high rate of complete closure but can be associated with serious complications. Onyx injection into the cavernous sinus has also been used, with excellent clinical and angiographic results.

image Intravenous: embolization with coils or Onyx (Saraf et al., 2010) is the treatment of choice in indirect fistulas (Fig. 33E.3).

image Parent vessel sacrifice: a last resort (Gemmete et al., 2009a, 2009b).

Brain High-Flow Arteriovenous Fistulas

Intracranial pial high-flow AVFs may be classified as:

Intracranial Pial Arteriovenous Fistula

An intracranial pial AVF is a rare cerebrovascular lesion that has only recently been recognized as a distinct pathological entity. According to a series reported by Halbach et al. (1989), pial AVFs account for 1.6% of all intracranial vascular malformations. Intracranial pial AVFs have a single or multiple arterial connections to a single venous channel. They differ from brain AVMs in that they lack a true nidus and differ from dural AVFs in that they derive their arterial supply from pial or cortical arteries and are not located within the dura mater (Hoh et al., 2001).

Pial AVFs can be congenital or may result from a traumatic injury (Lee et al., 2008). Little is known about their pathophysiological mechanisms. The clinical suspicion of pial AVFs should be followed by prompt appropriate treatment because of their natural history. They are associated with congestive heart failure, intracranial varices, increased intracranial pressure due to venous hypertension, and rarely with ICH.

Direct surgical exposure and occlusion of these vascular lesions is associated with high morbidity and mortality (Passacantilli et al., 2006). Today, most intracranial high-flow pediatric and adult AVFs are treated endovascularly. Accurate identification of the arteriovenous shunt and its precise occlusion with embolic materials make the neurointerventional approach the gold standard for this kind of cerebrovascular lesion.

Vein of Galen Aneurysmal Malformation

Vein of Galen aneurysmal malformations (VGAM) are rare intracranial AVFs that present almost exclusively in children. They are disproportionately represented in pediatric neurovascular disorders, accounting for up to 30% of intracranial vascular abnormalities (Gupta et al., 2006; Kumar et al., 2006). A VGAM consists of multiple AVFs draining into a dilated median prosencephalic vein of Markowski (Hoang et al., 2009). This embryonic vein does not drain normal tissue and does not communicate with normal cerebral veins. In many cases, the straight sinus is absent, and the vein drains directly into the superior sagittal sinus through the falcine sinus. VGAMs can be categorized into choroidal or mural, depending upon their arterial supply.

Clinical manifestations vary according to age:

The primary indication for treating neonates with VAGMs is congestive heart failure refractory to medical treatment (Horowitz et al., 2005). Elective embolization is performed to close the arteriovenous shunt by the arterial route (Bhattacharya and Thammaroj, 2003). Endovascular techniques include transarterial embolization with cyanoacrylate or Onyx, transvenous embolization with use of coils and Onyx, and combined techniques (Pearl et al., 2010) (Fig. 33E.4). Endovascular embolization has considerably improved outcomes in patients with VGAM. More recently, with the continued development and improvement of endovascular techniques, many patients are found to be neurologically normal on clinical follow-up, and mortality rates have dropped substantially when compared with microsurgical treatment (Khullar et al., 2010).