neuroendovascular management of tumors and vascular malformations of the head and neck

NeuroendovascularManagement of Tumorsand VascularMalformations of theHead and Neck
Laligam N. Sekhar, MD, FACSa,b,d,*, Arundhati Biswas, MDa,Danial Hallam, MDa,b, Louis J. Kim, MDa,b, James Douglas, MDc,Basavaraj Ghodke, MDa,b
KEYWORDS� Embolization � Onyx � Brain arteriovenous malformation� Dural AV fistulas � Tumors

Endovascular procedures are rapidly expandingas treatment options for cerebrovascular diseasesand neoplasms of the head and neck and arebecoming less invasive but more effective. Thereare potentially dangerous anastomoses betweenthe extracranial and intracranial circulations;hence, thorough knowledge of the anatomy isessential to minimize the risk of cranial nervepalsies, blindness, or neurologic deficits. It isessential to understand the scientific basis oftreatment rationale based on advancing new neu-roimaging techniques to better serve patients. Aninterdisciplinary approach and treatment in high-volume centers are vital to obtain maximal benefitfor patients.

Endovascular therapy has continuously evolvedand improved since it was first described in 1904.1

Rapid advances in the field have resulted in theability to safely embolize and effectively treat cra-niocervical neoplasms and vascular malforma-tions. Preoperative embolization of tumorsreduces intraoperative blood loss, shortenssurgical time, and decreases surgical morbidity.2,3

This technique involves superselective

a Department of Neurosurgery, Harborview Medical CBox 359766, Seattle, WA 98105-9950, USAb Department of Radiology, Harborview Medical Center,c Department of Radiation Oncology, Harborview Medicad Department of Neurological Surgery, Harborview Med* Corresponding author. Department of NeurologicalSeattle, WA 98104.E-mail address: [email protected] (L.N. Sekhar).

Neurosurg Clin N Am 20 (2009) 453–485doi:10.1016/j.nec.2009.07.0071042-3680/09/$ – see front matter. Published by Elsevier I

catheterization of the feeding arteries to the tumorbed with infusion of embolic particles to saturatethe tumor bed in the hopes of inducing necrosis.For some malignant head and neck tumors, selec-tive infusion of chemotherapeutic agents has beenperformed as part of combined therapy.

The endovascular therapy of brain arteriovenousmalformations (AVMs), dural arteriovenous fistulas(DAVFs), carotico-cavernous fistulas, and vein ofGalen malformations is part of the therapeuticstrategy. This article presents the indications,techniques, results, and potential complicationsof endovascular embolization of craniocervicalvascular malformations, and craniocervicaltumors.

BRAIN ARTERIOVENOUSMALFORMATIONSIndications for Treatment

Embolization of an AVM is mainly used as anadjunct to surgical treatment to reduce the sizeof an AVM or make it safer for surgery, althoughin some patients with small AVMs and a few arte-rial feeders, ‘‘angiographic cure’’ of an AVM may

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be possible.4–8 With surgically inaccessible AVMs,embolization may be used to eliminate perinidal orflow-related aneurysms as a prelude to radiosur-gery.9,10 With large AVMs that are not candidatesfor surgical treatment, embolization may be per-formed in stages to reduce the size of an AVMand render it suitable for radiosurgery, ina protocol-driven fashion (the efficacy of thismodality is as yet unproved). Several centers,however, have reported good preliminaryexperience.9,11,12

In general, any treatment of an AVM must offerpatients a significant advantage over the naturalhistory.13 In this regard, the combined mortalityand morbidity of procedures used must be consid-ered in making a treatment decision and discus-sing options with patients.

The authors classify AVMs as ruptured and un-ruptured, because the natural history is different.The rebleeding rate of a ruptured AVM is 6% forthe first year and 2% to 4% per year thereafter,whereas the bleed rate of an unruptured AVMhas been estimated from 2% to 4% (as low as2% and as high as 10%).14,15 In addition, AVMsare generally classified according to Spetzler-Martin (S-M) grade (Table 1).16 Although contro-versial, especially in regards to grade 3, whichencompasses a variety of AVMs, it is the mostwidely used grading system. In this regard, theauthors believe that the size of an AVM and itslocation (perirolandic, posterior fossa, or deep)are the most important variables determiningoutcome. The role of embolization-related compli-cations has been well correlated with increasingAVM grade.8,17,18 For S-M grades 1 and 2 AVMs,

Table1Spetzler-Martin grading score of AVM

Characteristic

Size of lesionSmall (<3 cm)

Medium (3–6 cm)

Large (>6 cm)

LocationNon eloquent

Eloquent sitea

Pattern of venous drainageSuperficial only

Any deep

Based on S-M grading system estimating the risk of surgery, wlocation. From Spetzler RF, Martin NA. A proposed grading sy65(4):476–83; with permission.

a Sensorimotor, language, or visual cortex; hypothalamus orcles or cerebellar nuclei.

embolization may be offered to mark an AVM fora surgeon (the black-colored Onyx [eV3, Irvine,California] is a good marker) to occlude an impor-tant feeding vessel that is surgically less acces-sible, to occlude a perinidal aneurysm, or toattempt to cure an AVM endovascularly. Withgrades 3 and 4 AVMs, embolization is usually per-formed in a staged fashion to reduce the risk ofpostoperative normal pressure perfusion break-through bleeding and to make surgery easier.Grade 5 AVMs are operated only under excep-tional circumstances. For grades 4 and 5 AVMs,embolization may be performed as a prelude toradiosurgical treatment.19

With ruptured AVMs, the timing of embolizationis a matter of variability and controversy.8,20 Inthe authors’ institution, patients with large clotsare often operated emergently (if they are herni-ating and if an AVM is small) or early (withina few days). In such patients, embolization maybe performed urgently if a surgeon desires. Inother cases, embolization is started as soon aspossible (without waiting for the clot to clear) andcontinued in stages (at approximately 2-weekintervals) until the desired level of obliteration isneeded.

Technique of Embolization—BrainArteriovenous Malformations

Many centers have reported the safety and effi-cacy of N-butyl cyanoacrylate (NBCA) and particleembolization for AVM treatment.21,22 Because ofthe well-documented handling characteristics of

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Head and Neck Neuroendovascular Procedures 455

Onyx, however, the authors’ institutional experi-ence focuses primarily on Onyx embolization.

The majority of brain AVMs are now embolizedwith the liquid embolic agent, Onyx, in two viscousconcentrations, Onyx-34 or Onyx-18. All emboli-zation procedures are performed with patientsunder general anesthesia in a biplane angio-graphic unit. Systolic blood pressure during theprocedure is controlled at less than 120 mm Hg.Post embolization, the blood pressure is kept10% lower than the baseline systolic pressure inchildren or less than 110 to 120 mm Hg in adultsafter the procedure for 24 hours. After preparingand draping the groins in a sterile fashion, thefemoral artery is accessed by an 18-gauge needleand, using the Seldinger technique, a 6-French (Fr)femoral sheath is inserted into the vessel andsecured. Diagnostic angiography is then per-formed using a 4-Fr vertebral catheter with viewsof the intracranial (IC) vessels in various projec-tions, including 3-D views, to delineate all feedersto an AVM and understand the dynamics of bloodsupply and venous drainage pattern. In someAVMs with rapid shunts, filming at high speed (6frames/s) may be required. Intra- and perinidalaneurysms are noted.

Patients are heparinized before embolization,usually with 5000 U intravenously, and 1000 Uper hour are repeated as needed to maintain theactivated clotting time at 300 seconds (50 mg/kgin children). The heparin is not reversed at theend of the procedure unless there is intraoperative

Fig. 1. Various types of feeder vessels to the AVM. (A) En p(B) Direct feeder to the AVM nidus. (C) Network of enlarg

perforation of the vessel or rupture of AVM. Theguiding catheter is constantly flushed via a pres-sure bag with saline, which does not contain anyheparin.

The first vessel chosen for embolization is usuallya direct feeder to the AVM (not feeding throughcollaterals and not an en passage vessel) with atleast 2 cm of safe distance available for refluxbefore cortical branches are reached (Figs. 1 and2A). A dimethyl sulfoxide (DMSO)-compatible mi-crocatheter (Marathon 1.3-Fr eV3) is navigatedinto the artery close to the nidus of the AVM withaid of a 0.008-in micro–guide wire (Mirage, eV3);multiple reshapes of guide wire may be needed toreach the target site. In some cases, when an arteryis large, a catheter may be able to be advancedalong the vessel close to the AVM with the wire re-tracted inside, to avoid perforation of a thin-walledartery. It is important to have the microcatheter tipas close to the nidus as possible and to havea good distance between the catheter tip and anynormal branch proximal to it (safe reflux distance).The safe reflux distance ideally should be at least2 cm and clearly noted in the roadmaps beforeembolization. The micro–guide wire is removedand biplane superselective angiography is per-formed through microcatheter to analyze theanatomy of the nidus segment and verify that onlythe AVM nidus is filled. During embolization, goodangiographic views of AVM in two projectionsshould be shown on the screen to see the tip ofthe microcatheter clearly, to appreciate the reflux

assage vessel giving branches on its way to the cortex.ed collaterals supplying the AVM.

Fig. 2. (A) Position of the microcatheter for Onyx embolization. Note the reflux of Onyx around the tip of the micro-catheter to form a plug. (B) Patterns for identifying nidal injection and venous injection during Onyx injection.

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readily, and to appreciate the anatomy of the AVMand the surrounding brain. Once embolization fromthis position is decided on, the microcatheter isover flushed with 10 mL of normal saline to clearany remaining contrast, then filled with 0.23 mLDMSO, and the catheter hub is also bathed inDMSO to clear the saline, because Onyx precipi-tates in contact with saline. Onyx is aspirated intoa 1-mL syringe and a connection is made to quicklyform a meniscus between the Onyx and DMSO.Onyx is injected slowly at a flow rate of 0.1 mL perminute to fill the microcatheter and replace theDMSO in the dead space. Embolization is usuallystarted with Onyx-34 (twice as viscous as Onyx-18) in order to form a plug around the catheter tip.Free flow of the Onyx is noted into the AVM nidusuntil there is a reflux noted. Embolization is per-formed with a gentle and steady push, or gentlesmall puffs, with progress viewed all the time. Insmall AVMs, significant penetration may occurwith the first push, before reflux occurs, so careshould be exercised. When reflux is noted, theoperator stops for varying periods of time (30seconds to 1 minute) before restarting. After first re-flux, anywhere from 2 to 10 minutes may be neededto form an adequate plug before the secondforward penetration occurs again. As this point isabout to be reached, forward and retrograde (bidi-rectional) flow often is observed.

Progress of embolization is followed by notingsingle radiographic exposures of the Onyx cast(and comparing with the AVM images) and inter-mittent angiographic runs to evaluate the AVMfilling (Figs. 3–10). For each embolizationsequence, a blank road map is obtained. Avoidingvenous embolization is important. When passingthrough a vein, Onyx tends to laminate initiallyalong the venous wall or quickly pass through tothe venous sinus. During embolization, filling of

the veins is noted by streaking or pooling, whichis an indication to stop for up to 1 minute. Theoperator must have a good understanding ofwhere the veins are inside the AVM and in itsperiphery to identify and avoid venous emboliza-tion. Reflux into normal brain areas around theAVM perimeter is an indication to stop for 30seconds. The maximal safe reflux distance alongthe feeding vessel should be judged on the initialangiogram (usually no more than 2 cm back or 1cm distal to a cortical branch of the feeding artery)and the fluoroscopy tube is appropriately posi-tioned during embolization to judge this rapidly,because the embolic agent filling the AVM mayinterfere with the initial views. After the initialembolization epochs, with the plug well formed,the operator may switch to Onyx-18, which isless viscous and penetrates the AVM more easily.

Endpoint of embolizationOperators should use judgment and experience toend an embolization session. With small AVMs, theentire AVM or the majority of the AVM is embolizedin one session. In such cases, the endpoint isreached when the major veins are filling (Fig. 2B).One should not try to achieve a perfect resultwith the sacrifice of safety, because this is whencomplications occur.

With large and giant AVMs, embolization isusually done in stages, with approximately 25%to 40% of the AVM embolized in the first session.The endpoint of an embolization session isreached when, after repeated pushes of embolicagent, no significant progress is noted. Theconsiderations are to embolize larger AVMs(>3 cm) in a staged fashion to achieve maximalbut safe reduction of the AVM volume and to emb-olize areas that are surgically difficult. The operatorstarts with direct feeders to the AVM (not en

Fig. 3. (A) MRI scan showing a 7-cm AVM in the frontal lobe bordering the sensorimotor cortex. (B) Angiogramsshowing a S-M grade V AVM. (C, D) Angiograms showing Onyx cast obliterating the posterior portion of the AVMbordering the rolandic fissure after four stages of Onyx embolization in 3 weeks. (E, F) Plain skull radiographsshow the embolized AVM.


passage feeders) and progresses to more surgi-cally difficult areas. During subsequent sessions,the goal of an embolization should be to embolizeregions that are more difficult for surgery (eg, themore posterior region in a perimotor AVM, thepart supplied by the PCA branches in a parieto-occipital AVM, or the portion supplied by ACA

feeders in a medial frontal AVM). With largeAVMs, 2 to 3 days before surgical excision, a largervolume of the AVM may be embolized, but patientsmust remain in the hospital with strict control of theblood pressure until surgical resection.

Although it is preferable to embolize the apicalportions of the AVM to make surgical excision

Fig. 4. Angiograms at 9 months showing complete removal of the AVM.

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easier, this is often difficult, in the authors’ experi-ence. As much as possible, intra- and perinidalaneurysms must be obliterated in the first emboli-zation session, especially in cases of rupturedAVMs. An embolization session is stopped when(1) the desired volume of embolization has beenreached, (2) there is repeated opacification ofdraining veins, (3) the maximum safe distance forreflux is exceeded, or (4) despite a moderate injec-tion pressure, there is no forward flow of Onyx.21

Management of vessel perforationDuring initial navigation of the microcatheter,penetration of the artery may rarely occur by guide

Fig. 5. MRI scans showing an AVM in the right sylvian fiss

wire or catheter. It can be recognized by an unex-plained position (relative to the arterial anatomy) ofthe wire or catheter or, in extreme cases, bychanges in a patient’s vital signs. It can beconfirmed by a small-volume contrast injectionthrough a microcatheter or by angiographythrough a guiding catheter. Once this is recog-nized, the catheter (or wire) must be left in placewhile the heparin is reversed with protamine. Afterreversal, while the microcatheter is withdrawn,a small (0.1 to 0.2 mL) volume of Onyx is injectedinto the artery to seal the perforation. Furtherembolization may be done through another vesselif the feeding artery is well sealed, the

ure and frontal lobe. (A) Axial; (B) Coronal.

Fig. 6. Angiograms showing a S-M grade IV AVM with deep venous drainage. (A) Right carotid injection, antero-posterior view; (B) Left ICA injection, anteroposterior view; (C) Right ICA injections, lateral view showing venousdrainage.


extravasation is minimal, and there are no changesin vital signs in a case of ruptured AVMs, ordeferred to another session in cases of largeextravasations, unstable vital signs, or unrupturedAVMs. During embolization, extravasation of Onyxalso may occur from the feeding artery, one of thedraining veins, or inside the AVM nidus. This canbe recognized by pooling and is an indication tostop the embolization.

Microcatheter withdrawalAt the end of the procedure, after aspirating withthe Onyx syringe, the microcatheter is pulledback slowly, increasing the tension on the tipduring withdrawal, holding the tension for a fewseconds, and repeating this maneuver a few timesuntil the microcatheter pulls out of the cast of Onyx

around it. During retrieval, protamine is kept readyfor reversal of anticoagulation should an acci-dental rupture occur, but the authors have neverhad to use it in their series of patients. Immediatelyafter retrieval of the microcatheter, the position ofthe guiding catheter must be checked because itcan easily migrate cranially. The guiding cathetershould be thoroughly aspirated to remove anyclots before performing post proceduralangiography.

Postoperative care of patientsPatients are monitored in an ICU, and the bloodpressure is kept 10% lower than the baselinesystolic pressure in children or less than 120 mmHg in adults for 24 hours to minimize the risk ofpostembolization hemorrhage. Femoral sheaths

Fig. 7. Angiograms (A, B) and plain skull radiograph (C) showing the obliteration of the medial portion of theAVM by Onyx cast.

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are usually removed on the following day and mostpatients are discharged home after 48 hours.

Hemorrhage from arteriovenousmalformations during or after embolizationand managementHemorrhagic complications are devastating andprobably occur due to inadvertent occlusion ofthe venous outflow during embolization withoutelimination of the arteriovenous shunt. Congestionof the nidus with slow-standing dye might beobserved. Embolization of multiple pedicles ata single setting may result in too rapid an alterationof the hemodynamic of the AVM and may result insubsequent hemorrhage. This can be avoided bystaged embolization. Finally, catheter/wire manip-ulation may cause vessel perforation resulting inintracerebral hemorrhage (ICH) or subarachnoidhemorrhage (SAH). This can be minimized by

limiting the use of guide wire to selecting thedesired proximal pedicle while letting the naturalflow characteristics of the AVM carry the pliableflow-directed microcatheter to the distal positionfor embolization. Immediate reversal of heparinwith protamine and termination of procedure isrequired in arterial perforation with unstableparameters.

Arteriovenous fistulaeWith very high-flow AVMs and arteriovenousfistulae, it may be necessary to use a largerOnyx-compatible microcatheter (Echelon 10 orEchelon 14, eV3) to allow the placement of coilsinto the vessel to arrest or slow the flow. Thismay be followed up with the liquid embolic agent.During such procedures, significant hypotension(down to 60-mm systolic blood pressure) or aden-osine-induced brief cardiac arrest may be used. In

Fig. 8. Angiograms obtained at the time of follow-up showing complete obliteration of the AVM nidus. (A)Lateral view, right ICA injection; (B) Anteroposterior view, right ICA injection.


such cases, monitoring of somatosensory evokedpotentials (SSEP) and motor evoked potentials(MEP) is helpful.

Clinical Experience and Outcome

In a series of patients treated by the authors’ teamfrom August 2005 to October 2008 at the theirinstitution, a total of 128 patients were treateddefinitively, 4 by embolization alone, 60 by embo-lization and microsurgery, 14 by embolization andradiosurgery, 7 by all three modalities, and 43 byonly surgical removal or radiosurgery.

From the total of 128 patients, 60 presented withrupture of the AVM and ICH or SAH. In a subset of75 patients treated with embolization, complica-tions were noted in 10 (Table 2). One patientdeveloped left-sided hemiplegia 8 hours afterembolization of a S-M grade V AVM in the occipi-totemporal region through feeders from the ante-rior choroidal artery. She had an infarct in theright occipitoparietal and thalamic region on MRI.The AVM was surgically removed, but the patientremains disabled (modified Rankin score [mRS]3). A second patient had an arterial perforationby the micro–guide wire that was managed byimmediate reversal of heparin with protamineand termination of the procedure. She wassuccessfully embolized the next day and hadcomplete microsurgical resection after 2 moredays. She had no neurologic deficits. Two patientshad stuck microcatheters after embolizations thatwere left in situ; they were identified intraopera-tively and extracted in both cases. There weretwo deaths of patients who did not recover aftertheir bleed, unrelated to the treatment.

At 3 months, 63% recovered with no or milddisability. The outcome as measured by mRSswere slightly better in the radiosurgery seriesthan in the microsurgery series in AVMS withS-M grades I to III but this difference was notsignificant (P 5 .583). One patient from the radio-surgery group had recurrent bleed in the interimperiod (Table 3).

Case Examples of Embolized ArteriovenousMalformations

Patient 1An 8-year-old girl presented with recurrent tinglingsensations on the left side of the body and weak-ness of the left arm and leg. She was found tohave a S-M grade V AVM measuring 7.0 � 4.5 �2.8 cm in size, involving the motor area. Emboliza-tion was aimed at the apex and the posterior partbordering the sensorimotor cortex parts of theAVM that were more difficult to manage withsurgery. Onyx embolization was performed infour sessions over 3 weeks. The posterior portionof AVM bordering the rolandic fissure was embol-ized, but the apex could not be embolized.Surgical resection was elected because of heryoung age, which creates a greater potential forcerebral plasticity because she was likely tocompensate for any deficits sustained at thetime. The AVM was excised completely 4 daysafter the last stage of embolization. Postopera-tively, she had increased weakness that graduallyimproved. At follow-up 3 years later, she hadnormal school and intellectual performance buta slight weakness of her left upper extremity with

Fig. 9. Angiogram reveals a moderate-sized AVM with feeders from the MCA and drainage in to the superior sag-gital. (A) Left ICA injection, anteroposterior view, arterial phase; (B) Lateral view, arterial phase; (C) Anteropos-terior view, venous phase; (D) Lateral view, venous phase.

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mRS 1, and angiography showed completeremoval of the AVM.

Patient 2A 52-year-old woman presented with recurrentsevere headaches. She was found to have a S-Mgrade IV AVM in the right sylvian fissure, the basalganglia, and the frontal lobe (see Figs. 5 and 6).Embolization was performed with Onyx in foursessions over 4 weeks, aiming at the medialportion of the AVM in the basal ganglia (seeFig. 7). Surgery was performed 2 days after the

last embolization, and the AVM was removedcompletely. The patient had left hemiparesis post-operatively and had inpatient rehabilitation. Ata follow-up examination 8 months after surgery,power in all four limbs was normal, and she had re-turned to her normal activities and work (mRS 1).Angiography 8 months after surgery showedcomplete obliteration.

Patient 3A 22-year-old man presented with seizures. Onimaging, he was found to have left frontal S-M

Fig.10. Progression of the Onyx cast in various stages seen filling the AVM. Figures A–E are images of the ONYXcast during the embolization.


grade 3 AVM in the premotor area. He was sub-jected to two sessions of embolization with Onyxfollowed by surgical resection. Patient hada complete recovery with no symptoms at follow-up (mRS 0).

Patient 4A 39-year-old man presented with intraventricularhemorrhage and on imaging was found to havethalamic AVM. The source of hemorrhage wasa small perinidal aneurysm, which was then em-bolized to eliminate immediate rebleeding risk.He was subsequently referred for radiosurgeryand patient is being followed up.

Patient 5A 52-year-old man developed severe headachesecondary to SAH with left cerebellar intraparen-chymal hemorrhage due to AVM rupture. Angiog-raphy demonstrated a left cerebellar complex,racemose hemispheric arteriovenous malforma-tion, predominantly fed by branches of the leftposterior inferior cerebellar artery (PICA) witha perinidal aneurysm on the superior branch ofthe left PICA feeding into the AVM. Because ofthis, there was high risk of immediate rebleedand patient was planned for immediate emboliza-tion. He underwent preoperative embolization intwo stages followed by surgical resection of theAVM and clipping of the superior cerebellar artery(SCA) aneurysm. Patient had a good recovery andwas mRS 2 at follow-up.

DURAL ARTERIOVENOUS FISTULAS

IC DAVFs are acquired abnormal arteriovenousconnections within the dura that account for 10%to 15% of all IC AVMs (Figs. 11–23).23 Most lesionsmay develop as a consequence of venous sinusthrombosis and the attempted recanalization butsome congenital DAVFs have also been described.There is a female preponderance with symptomsusually developing during middle to late adulthood.A presentation with aggressive neurologic symp-toms is more common in men.24,25

Previous surgery, ear infection, and headtrauma have all been cited as potential causes,although the common predisposing factor seemsto be venous sinus thrombosis.26,27 Venousthrombosis promotes venous hypertension, whichacts as the initiating factor opening up micro-scopic vascular connections within the dura.Maturation of these channels secondary toprogressive venous stenosis or occlusion resultsin the development of direct shunts between thearteries and dural veins.28,29 In addition, a secondcomplementary mechanism of DAVF evolutionmay occur with the release of angiogenic growthfactors, such as vascular endothelial growth factor(VEGF) and basic fibroblast growth factor,promoting neovascularization and developmentof a DAVF.30 Lasjaunias and Berenstein have sug-gested ‘‘an underlying dural weakness’’ facilitatingdural shunts in some individuals.31 In children,DAVFs may occur as congenital lesions, with

Table 2Complications of embolization

Embolization No. of Patients

Thromboembolic event leading to hemiplegia 1

Vessel perforation 1

Infection 1

Vein of Labbe stenosis 1

Stuck catheter 2

Failed catheterization 3

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a presumed cause of venous thrombosis in fetallife or abnormal development.

Symptoms

DAVFs may be asymptomatic or present withsymptoms that are mild to severe. Severe symp-toms include ICH, visual loss, focal neurologicdeficits, dementia, and eye pain or diplopiasecondary to venous hypertension. Minor symp-toms may include headache, tinnitus, dizziness,trigeminal neuralgia, hemifacial spasm, and soforth. Drainage of a petrous region DAVF to thetransverse or sigmoid sinus commonly producespulsatile tinnitus or hearing loss, sometimes inassociation with an audible bruit. Other cranialnerve (CN) symptoms (trigeminal neuralgia andhemifacial spasm) may be caused due to

Table 3Modified Rankin score outcome based onmodality

Modified Rankin Score

EmbEmbSurgN 5

0. No symptoms at all 25 (

1. No significant disability despite symptoms;able to carry out all usual duties andactivities

24 (

2. Slight disability; unable to carry out allprevious activities, but able to look afterown affairs without assistance

12 (

3. Moderate disability walks withoutassistance

6 (8

4. Moderately severe disability; unable towalk without assistance and unable toattend to own bodily needs withoutassistance

5 (7

5. Severe disability requiring care 2 (3

6. Dead 2 (3

compression by an enlarged artery or drainingvein. Cavernous sinus DAVFs may develop orbitalsigns, such as congestion, chemosis, and ophthal-moplegia.32,33 More aggressive behavior maymanifest as focal neurologic deficits, dizziness,a dementia-type syndrome or cerebral hemor-rhage, including subarachnoid, subdural, or intra-parenchymal bleeds. Such features are usuallyconsidered due to venous hypertension.

The most common location of cranial DAVF istransverse-sigmoid sinus followed by thecavernous sinus.34–36 In a meta-analysis of 360DAVFs, the tentorial incisura was the mostominous location, with 31 of 32 cases associatedwith hemorrhagic or nonhemorrhagic stroke.32

The venous drainage pattern is the most importantpredictor of the clinical behavior, however, andthose with retrograde leptomeningeal drainage

olization/olization Dery/surgery (%)76

Embolization DRadiosurgery/Radiosurgery (%)N 5 52

Total No. ofPatients (%)N 5 128

33) 14 (27) 39 (31)

32) 20 (39) 44 (34)

16) 7 (14) 19 (15)

) 6 (12) 12 (9)

) 3 (6) 8 (6)

) 2 (4) 4 (3)

) 0 (0) 2 (2)

Fig. 11. After two stages of embolization, more than 70% obliteration of the AVM with only a small residualportion seen inferiorly (arrows). (A) Anteroposterior view, left ICA injection; (B) Lateral view, left ICA injection.


exhibit a much higher incidence of hemorrhage orvenous infarction. The annual mortality rate fora DAVF with cortical venous reflux (CVR) may beas high as 10.4%, whereas the annual risks forhemorrhage or nonhemorrhagic neurologic defi-cits during follow-up are 8.1% and 6.9%, respec-tively, resulting in an annual event rate of 15%.Moreover, rebleeding rates may be as high as

Fig.12. Postoperative angiography shows complete resectioroposterior view; (B) Lateral view.

35% over the first 2 weeks after the initial hemor-rhage.37,38 Thus, these formidable lesions needcareful evaluation and rapid treatment.

The preliminary diagnosis of DAVF is based onclinical presentation. After initial suspicion, CTand CT angiography or magnetic resonance angi-ography may be performed. Angiography isneeded for definitive diagnosis. The projections

n of AVM with no residual AVM nidus seen. (A) Ante-

Fig.13. (A) Left ICA injection; left thalamic AVM (white arrow) with perinidal aneurysm (black arrow) and nidusmeasuring approximately 2.4 cm � 1.4 cm � 1.7 cm centered in the left thalamus with left P1, P2, and P3 segmentarterial feeders and drainage via the vein of Galen. (B) Three dimensional image of the left ICA injection showingthe aneurysm; (C) Vertebral injection showing supply to AVM and drainage.

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must include bilateral external carotid artery (ECA)runs, internal carotid arteries (ICAs), and bothvertebral arteries (VAs) if necessary. For lesionsaround the foramen magnum, upper cervicalarea, thyrocervical, and ascending cervicalarteries should be studied after an initial subcla-vian injection.

The Borden system of classification iscommonly followed for classification and treat-ment indication, but the Cognard system is moredetailed (Tables 4 and 5).

Treatment Philosophy and Algorithm

The primary goal of treatment is the completeobliteration of the lesion. In some cases, however,palliative treatment for control of symptoms may

be performed. The therapeutic armamentariumincludes conservative monitoring, arterial emboli-zation, transvenous occlusion, surgical excision,and radiation therapy. In current practice, manylesions can be eliminated by an endovasculartechnique. The main goal of endovascular treat-ment of aggressive DAVFs is to eliminate thecortical venous drainage and the resulting risk ofICH. Different endovascular approaches can beused in the treatment of these lesions.

In Borden 1 cases, treatment is needed only forseverely symptomatic cases, and palliative(incomplete treatment) is an option. The aim oftreatment in such lesions is cure, but palliationcan be accepted to reduce the morbidity. In Bor-den 2 and 3 cases, treatment is mandatory, andwhen a patient presents after an acute ICH,

Fig.14. (A) Carotid angiogram; reduction in the size of AVM and presence of Onyx cast (white arrow) post embo-lization. (B) CT angiogram; (C) CT scan without contrast.


treatment should be provided as soon as possible,to prevent the prospect of rebleeds. The goal isto occlude the fistula in all DAVFs, and especiallyto occlude the origin of the draining vein to preventrecurrence in Borden 3 fistulas. When endovascu-lar treatment is difficult or has failed, then micro-surgery is done as an alternative.39,40 In somedifficult cases, radiosurgery may follow the embo-lization procedure. In the authors’ center, transar-terial embolization with Onyx is used as theprimary treatment modality unless there are arte-rial branches supplying CNs, predominant ICAfeeders, or potential extracranial (EC)-IC collateralanastomosis. The transvenous technique is usedin cases of type 2 DAVFs where transarterialaccess is not possible or where combined transar-terial and transvenous treatment is needed. Thegoal of transvenous access is to enter the fistula

pouch from the venous side for coil embolizationat the point of the fistula itself. In some cases ofBorden 3 fistulas, the fistula can be accessedthrough the transvenous route.41

Surgical treatment is reserved in the authors’center for emergent clot evacuation and for caseswhere endovascular treatment is not possible orincomplete. A complete devascularization of thefistula or the occlusion of all the draining veins/vein of the fistula must be feasible for surgery tobe successful.41 Radiosurgery is performed asa last resort, for some cases of fistulae that cannotbe optimally treated by one of the techniquesdescribed previously, usually after embolizationor surgical resection. Radiosurgery takes 2 to 3years to obliterate the DAVFs and, until the lesionis completely obliterated, there is still a risk ofbleeding or other symptoms.42,43

Fig.15. S-M Grade 3 AVM within the left cerebellar hemisphere with arterial feeders from left AICA/PICA trunk,with small feeding branches from left superior cerebellar, and posterior cerebral arteries (A, B). Multiple smallfeeding artery perinidal aneurysms located close to the AVM nidus posteriorly (C).

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Case Examples of Embolization Techniquefor Dural Arteriovenous Fistulas

Case 1: transvenous embolization of anindirect carotid-cavernous fistulaA 49-year-old man presented with headache andproptosis and was found to have an indirectcarotid cavernous fistula (Borden 2) with bilateralmeningohypophyseal trunk (MHT) feeders andleft ECA feeders draining into the cavernous sinus,superior ophthalmic vein, and superior petrosalsinus. Complete obliteration of the fistula and reliefof all symptoms was achieved after transvenouscoil embolization of the cavernous sinus throughthe left superior petrosal sinus. This procedurewas under general anesthesia, a 6-Fr sheath wasplaced in the femoral artery, and angiography

was performed as needed during the procedure,using a 4-Fr vertebral catheter. The femoral veinwas punctured, a 6-Fr sheath inserted, and a6-Fr main pancreatic duct catheter negotiatedinto the internal jugular vein. An Excelsior SL-10microcatheter (Boston Scientific, Natick, MA)with a Synchro 14 microwire (Target Therapeu-tics/Boston Scientific, Fremont, California) wasthen used to superselectively catheterize the leftsuperior petrosal sinus and ultimately the leftcavernous sinus. The catheter was positionedanteriorly at the junction of the left ophthalmicvein and multiple entering arterial fistula pediclesand multiple guglielmi base detachable (GDC)360 platinum coils were deployed within the ante-rior left cavernous sinus. Occlusion of the fistulawas confirmed by transarterial angiography.

Fig. 16. (A) Postembolization showing significant reduction in the size of AVM. Postoperative angiography showsa complete resection with aneurysm clip seen in situ (arrow) (B, C).


The cavernous sinus is usually entered by navi-gating a microcatheter through the inferior orsuperior petrosal sinus. Rarely, when such accessis not possible, and when there is predominantanterior drainage, catheterization can be via thesuperior ophthalmic vein or a facial vein. The supe-rior ophthalmic vein can be exposed by a cut-down technique.

Case 2: transarterial Onyx embolizationof convexity dural arteriovenous fistula(Borden 3)A 60-year-old man presented with headache andwas found to have an ICH. Cerebral angiogramshowed a convexity osteo-DAVF with feedersfrom bilateral occipital artery, middle meningealtrunk, and right posterior cerebral artery. The

venous drainage was predominantly into menin-geal and cortical vein and into the middle third ofsuperior sagittal sinus. There was partial narrowingof the superior saggital sinus and with venouscongestion on bilateral ICA injections. Transfemor-al access was achieved using a 6-Fr sheath underanesthesia. Superselective catheterization of theECA was done using a 5-Fr Envoy catheteradvanced over a 0.035 in glidewire. Using roadmapping guidance, a Marathon 1.3-Fr microcath-eter was advanced over a Mirage 0.008 microwire,and transarterial Onyx embolization was per-formed in three sessions through bilateral poste-rior branches of middle meningeal trunks andright occipital artery. There were no complicationsor CN palsies and the fistula was completelyobliterated.

Fig. 17. Cerebral angiogram showing an indirect carotid-cavernous fistula (Borden type 2) with bilateral MHTfeeders (A, B) and left ECA feeders (C, D) draining into the cavernous sinus, superior ophthalmic vein and superiorpetrosal sinus (arrow).

Fig.18. (A) Tranvenous access to the fistula site through the left superior petrosal sinus. (B) Postembolization cere-bral angiogram showing complete obliteration of the fistula.

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Fig.19. (A) Noncontrast head CT showing an intracerebral hemorrhage. Cerebral angiogram showing a convexityosteo-DAVF with feeders from bilateral occipital artery, middle meningeal trunk (B, C) and right posterior cere-bral artery (D). Venous phase of cerebral angiogram showing partial narrowing of the superior sagittal sinus andwith venous congestion on bilateral ICA injections (E, F).


Case 3: Onyx embolization of tentorialarteriovenous fistula (Borden 3)An 85-year-old woman presented with headacheand was found to have a posterior fossa hemor-rhage on CT scan. Cerebral angiogram showed

a tentorial DAVF supplied by feeders from bilateraloccipital artery and left posterior meningealbranches. The venous drainage was into a tentorialvein that had a venous aneurysm and drained intothe transverse sinus. A 6-Fr KSAW Shuttle-Select

Fig. 20. (A) Postembolization angiogram showing Onyx cast (arrow) and (B) complete obliteration of the fistula.

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(Cook, Bloomington, Indiana) introducer sheathwas placed in the left ICA and using a Echelon10 and Mirage 0.008 inch guide wire, competeobliteration of the fistula was achieved after

Fig. 21. (A) Noncontrast head CT showing posterior fossaDAVF supplied by feeders from bilateral occipital artery (B,drainage was into a tentorial vein that had a venous ane

transarterial embolization with Onyx-18 throughthe dural branch of the occipital artery. The cath-eter was stuck in the occipital artery, broke ata point 10 cm from the tip, and was deposited in

hemorrhage. Cerebral angiogram showing a tentorialD) and left posterior meningeal branches. The venous

urysm and drained into the transverse sinus (C).

Fig. 22. Cerebral angiogram with selective left occipital artery injection (A). Postembolization angiogram showingcomplete obliteration of the fistula (B, C) and the retained stuck catheter (D).


the occipital artery after cutting the catheter justunder the femoral skin edge.

Results and Complications

In the authors’ institution, 32 patients with DAVF(Table 6) were treated over 3.5 years between May2005 and December 2008 by endovascular emboli-zation (transarterial embolization with Onyx, trans-venous embolization GDC coils), surgery, orradiosurgery. Most common presentation washemorrhage (n 5 11), headaches, tinnitus, andorbital symptoms. Twenty-eight patients weretreated by endovascular embolization. Five patients(after incomplete-1 patients/failed-4 patients embo-lization) had surgical excision of the fistula. Threepatients were treated with gamma knife radiosur-gery after partial obliteration of fistula with Onyx.

The distribution of patients according to Bordenclassification was I, 6 (18.8%) patients; II, 13(40.6%) patients; and III, 13 (40.6%) patients.

Twenty-six of 32 (81%) patients had their fistulascompletely obliterated after multimodality treat-ments at 1 to 36 months’ follow up. Of the sevenpatients with residual after endovascular emboli-zation, four patients had surgical obliteration ofthe fistula and three underwent gamma knife ra-diosurgery. Surgical complications includedcognitive deficits with word-finding difficulty inone and seizures in another. At follow-up (3–36months), 15 patients had mRS 0–2, four patientshad mRS 3–5 (three due to the initial insult of thehemorrhage), and two patients were dead. Onepatient with a tentorial DAVF was attempted tobe embolized by a transvenous technique, butthe microwire was stuck to the vein during attemp-ted extraction and caused its rupture resulting inmassive hemorrhage and death. The other patientdied after an accidental fall and consequentsubdural hematoma (Table 7).

Transarterial embolization with Onyx hasincreased obliteration rates with low morbidity.

Fig. 23. (A, B) Postgadolinium T1-weighted coronal and saggital images showing a large right superior frontalmeningioma with partial extension across midline into the left frontal region.

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Surgical obliteration of the draining vein remainsan important treatment option for fistulas notaccessible through the endovascular route or afterfailed endovascular treatment.

EMBOLIZATION OF CRANIOCERVICALTUMORS

Tumors of the craniocervical area are embolizedmainly to make surgical resection easier, byreducing the bleeding during surgery, and some-times, also by making them softer by inducing in-tratumoral necrosis (Figs. 24–34). Rarely,embolization can be used as a palliative modalityto cause symptomatic improvement.2,44–46

Because embolization is part of the multimodaltreatment, it should be done with minimal risk,avoiding new CN deficits, stroke, or hemorrhage.Adequate devascularization of a tumor can rarelybe produced without embolizing all the importantfeeders and the nidal portions of the tumor dueto the presence of intratumoral collateral

Table 4The Borden classification system

1 Venous dra

2 Venous dra

3 Venous dra

Data from Borden JA, Wu JK, Shucart WA. A proposed classifimalformations and implications for treatment. J Neurosurg 19

circulation. The vascularity of the tumor is oftenmulticompartmental, as it is supplied by differentarteries, but the intratumoral vessels do communi-cate with each other. At the conclusion of emboli-zation, the feeding arteries may be occluded closeto the tumor.47

Tumors that are considered for embolization areusually large and extra-axial, although emboliza-tion also may be performed of intra-axial tumors,such as hemangioblastoma, choroid plexus papil-loma, or intraventricular meningioma, when thefeeding arteries can be safely accessed. Extra-axial tumors considered for embolization can bedivided into (1) convexity and parasagitta and (2)skull base tumors, the latter being technicallymore difficult.34 In addition to intratumoral emboli-zation, an endovascular surgeon may be asked toassess the risk of arterial sacrifice before or duringsurgery by the performance of a carotid occlusiontest. Occlusion testing of a venous sinus is not safeand has been accompanied by a disastrous

inage directly into dural venous sinus, no CVR

inage into dural venous sinus with CVR

inage directly into subarachnoid veins (CVR only)

cation for spinal and cranial dural arteriovenous fistulous95;82:166–79.

Table 5The Cognard classification system

Type I Drainage into a dural sinus, with normal antegrade flow

Type II Drainage into a dural sinus, with reflux intoII a: (other) sinusesII b: cortical veinsII a 1 b: sinuses 1 cortical veins

Type III Drainage into cortical veins

Type IV Drainage into cortical veins with cortical ectasia

Data from Cognard C, Gobin YP, Pierot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlationwith a revised classification of venous drainage. Radiology 1995;194:671–80.


complication in the senior author’s experience(L.N. Sekhar, MD, unpublished data, 1992).

As with embolization of AVMs, endovascularsurgeons and microsurgeons must communicateeffectively to understand the goals of the emboliza-tion and the permissible risk before the procedure.

Embolization Technique

Diagnostic angiographyGeneral endotracheal anesthesia is preferred for allembolization procedures, although in cooperativepatients, and when a single vessel is embolized,local anesthesia with conscious sedation can beused. Using the Seldinger technique, a 4-Fr sheathis inserted into the femoral artery and secured. Withthe assistance of a microcatheter and micro–guidewire, the appropriate first- or second-order vesselis selected and catheterized with a 4-Fr vertebralcatheter. Standard practice, for most large tumors,is to perform a diagnostic angiogram of both ICAs,both ECAs, and one dominant VA to document thestatus of the anterior and posterior communicatingarteries. Based on a tumor’s location, all potentialsources of blood supply must be studied, and anydangerous anastomoses between ECA and ICAor VA branches must be ruled out. 3-D angiographymay be used to better delineate the feeding vesselbut, in some cases, superselective angiography of

Table 6Location of dural arteriovenous fistula

Location

Transverse-sigmoid

Petrotentorial

Parasaggital/falcine

Anterior fossa

Middle fossa

Torcula

Carotico-cavernous fistula

the feeding vessel with a microcatheter may berequired, although this is usually best performedonce a decision to proceed with embolization ismade. Venous assessment is important whena tumor is compromising the dural sinus or jugularvein.48

Carotid occlusion testIf an ICA is encased by a tumor, particularly if it isencased and narrowed, then an assessment ofcollaterals may be requested by the operatingsurgeon. Two levels of assessment may be per-formed. In the authors’ center, a surgical sacrificeof the ICA is rarely done without a concurrentbypass procedure. In such a case, the authorsperform only a carotid compression angiogram.Cerebral angiography with manual ipsilateralcommon carotid compression with contralateralICA injection (anteroposterior view needed, focuson venous phase, filling, and emptying) demon-strates the potential cross flow through the anteriorcommunicating artery. A delayed venous filling andemptying is the best evidence of poor collateraliza-tion. An Alcock’s maneuver, which involves carotidcompression during injection of the dominant VA(anteroposterior and lateral views show the entireskull for lateral view), can show the posteriorcommunicating artery and potential collateral

No. of Patients

10

8

3

1

2

1

7

Table 7Complications of endovascular procedure

Endovascular Complications No. of Patients

Stuck catheter 3

CN palsy (V/VII) 1

Rupture of vein with death 1

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flow. A carotid occlusion test is performed with thepatient awake. The ICA is occluded in the C1-C2segment with a 7-mm � 7-mm HyperForm ballooncatheter (Micro Therapeutics, Irvine, California)through a 6-Fr guiding catheter for 30 minutes aftersystemic heparinization, and patients are observedfor any neurologic deficits.49 The authors also usetranscranial Doppler monitoring of the ipsilateralmiddle cerebral artery during the balloon testocclusion. A 30% drop in velocities with the ballooninflated indicates only borderline collateralization,and a 40% decrease indicates that the degree ofcollateral flow is probably inadequate to supportcerebral perfusion. It is also helpful to have patientson aspirin (325 mg) for 1 day preoperatively.50

Embolization

Once a decision is made to proceed with emboliza-tion, patients are heparinized. For ECA emboliza-tion, a 4-Fr vertebral catheter is used as a guidingcatheter. Usually, a Renegade 0.021 inch ID micro-catheter (Boston Scientific) with a 0.014 inch or0.016 inch hydrophilic micro–guide wire (for 350-to 500-mm polyvinyl alcohol [PVA] particles) or

Fig. 24. An irregular area of moderate tumor blush is projecthe frontal division of the right middle meningeal arteryadjacent superior sagittal sinus (B).

a Marathon microcatheter with a Mirage 0.008inch guide wire (for 45- to 150-mm PVA particles)is navigated into the vessel of interest, as distallyas possible, and beyond any important potentialcollaterals. In case of the middle meningeal artery,the operator needs to get past the petrosal branch,which supplies the facial nerve. With any ECAembolization, all collaterals to the ophthalmic arteryshould be studied carefully and avoided, becausesometimes the opthalmic artery has an aberrantorigin from the MMA. With the microcatheter inplace, superselective angiography is performed tostudy the microvasculature, intratumoral collat-erals, and the ease of reflux. The microcatheter isflushed with saline before the embolic agent isintroduced. For ICA or VA branch embolization,arterial road maps are needed; therefore, the 4-Frsheath is exchanged for a 6-Fr sheath, and a 6-Frguide catheter is used.

The most common embolic agent is PVA parti-cles, mixed with contrast material. Particles, sizes150 to 250 mm, are used for better penetration oftumor supply.47,51 In the case of ascendingpharyngeal or posterior auricular artery emboliza-tion, however, which may be giving rise to the

ted over the right frontal lobe supplied primarily from(A). A large area of filling defect is present within the

Fig. 25. Near complete stasis of flow within the frontaldivision of the middle meningeal artery with signifi-cant decrease in the previously noted tumor blushoverlying the right frontal lobe.


neuromeningeal trunk supplying the CNs 9, 10,and 11, 350- to 500-mm particles are used. Thisavoids penetration of the fine blood vessels (vasanervosum) supplying the nerves and attendantCN paralysis.52,53 Embolization is performed insmall puffs, with repeated road maps as necessaryand continuous fluoroscopic observation, untilstasis of contrast within the tumor is noted. Atthis point, the embolic syringe is replaced withsaline, which is used to gently push out thecontrast-particle mixture remaining inside thedead space of the microcatheter. In some casesof ECA embolization, the feeding vessel isoccluded with Gelfoam torpedoes using Rene-gade microcatheter. Gelfoam supplied in sheetsis cut into strips, approximately 1- to 2-mm wideand 2- to 3-mm long, and then rolled so that theyare very thin. They are then loaded into the huband the distal part of a 1-mL syringe, which is con-nected to the microcatheter, and injected.2,47,51

They produce rapid occlusion of the feedingarteries, but recanalization occurs in approxi-mately 6 weeks. The liquid embolic agent, Onyx,may also be used in cases of very vascular tumors;in such cases, the embolizaation technique issimilar to that used for AVMs.

Embolization through the MHT is important indevascularizing clival meningiomas. Whensuccessful, and combined with embolization ofany ECA feeders, this is effective in reducing theblood loss from these tumors.54 The cannulationof the MHT may be technically demanding, oftenrequiring 3-D angiography to understand the exactpoint of origin of the artery from the cavernous ICAand some probing with a microwire, with reshap-ing as needed. A Marathon 1.3-Fr microcatheterand a Mirage 0.008 microwire are used to cannu-late the MHT, taking the microwire at least 5 mmpast the origin of the MHT. Once cannulated withthe microwire, difficulty may be encountered withthe introduction of the microcatheter due to thesize of the vessel or the angle of take off. Whenthe microcatheter is well into the artery, it shouldbe wedged at its branch point or slightly pulledback. Embolization is performed carefully, andwith the smallest particles, to avoid reflux intothe ICA and downstream embolization.

Embolization by Direct Punctureof the Tumor

This technique is rarely used when a tumor is diffi-cult to access by the transarterial route but can beeasily accessed by direct puncture.55,56 Examplesof this case are angiofibromas, paragangliomas,hemangiopericytomas, some tumors of theconvexity, some jugular-mastoid tumors, and juve-nile nasopharyngeal angiofibromas, particularlywhen the feeding arteries are not accessible dueto previous procedures. The lesion is accessedthrough a prior craniotomy or a preauricular or pre-condylar area.57 After selective transarterial angi-ography, the lesion is punctured and directangiography is performed with and without manualcompression of the venous drainage in the regionand under fluoroscopic or ultrasound guidance.After the tumor is punctured, a contrast medium isinjected through the needle to identify the corre-sponding tumoral compartment and its drainingvein. Embolization is then performed with a mixtureof NBCA (Cordis Neurovascular, Miami, Florida)and lipiodol (Guerbet France, Paris, France), in-jected using a 3-mL syringe under fluoroscopiccontrol. NBCA and lipiodol are mixed in 1:3 propor-tions to which some powdered tungsten is added.With lipiodol, the progressive filling of the tumoralcompartment can be followed visually with fluoros-copy. Several intratumoral injections are necessaryto fill the tumor as completely as possible. Hence,the needle is withdrawn after each injection to reachanother tumoral compartment. Each intratumoralinjection must be slow and progressive, lastingfrom 20 to 30 seconds according to the size of the

Fig. 26. Meningioma, primarily supplied by the right MHT (C), right middle meningeal artery, distal branch of theright internal maxillary artery (likely deep temporal) (A, B), and left MHT.

Sekhar et al478

tumoral compartment. The injection is stoppedwhen the NBCA starts to flow into the drainingvein. In some cases, protection of ICA or VA isnecessary with a balloon while using direct punc-ture embolization.

When Not to Embolize

The presence of dangerous EC-IC anastomoses,shared arterial supply between tumor and normalstructures, the caliber of tumor vessel, and thepotential for the embolic particles to reflux intothe parent vessel are all factors that need to beconsidered before a decision to embolize.52,53

Pial vessels are fragile and thus associated with

a high risk of arterial perforation and IC hemor-rhage.58 The potential for stroke due to thrombo-embolism when embolizing through pial vesselsis also higher than when embolizing through ECAbranches. If a major tumor blood supply is derivedfrom small ICA branches or the ophthalmic artery,complete devascularization using microcathetersis not possible without unacceptable risk.

Complications of Intratumoral Embolization

Most common complications noted are fever andlocalized pain. Potentially more devastatingcomplications include focal neurologic deficitsdue to inadvertent passage of embolic material

Fig. 27. Particle embolization of the right distal internal maxillary artery, right middle meningeal artery (A), rightaccessory meningeal artery, and right MHT feeding branch (B) with no residual significant tumor blush from theright ECA branches and very little residual tumor blush from the right ICA postembolization.


through reflux or from ECA branches throughdangerous collateral anastomoses into the ICA orVA circulation,47,50,52,53 and intratumoral hemor-rhage. Embolization in the vascular territory ofthe ophthalmic artery carries a risk of blindness.59

Cutaneous branches of the ECA may be occludedcausing skin necrosis, thus complicating theprospective wound healing process.59,60 TransientCN palsies (provided particulate reabsorbableembolic materials are used instead of polymerizingfluid materials) can also occur due to interruption

Fig. 28. MRI showing a hypervascular recurrent hemangioCoronal.

of the vascular supply (vasa vasorum), which isoften derived from ECA.47,52 The petrous branchof MMA supplies the facial nerve and the neuro-meningeal branch of the ascending pharyngealartery supplies CNs 9 through 12 and can be inad-vertently embolized. Tumor swelling post emboli-zation may compromise the airway or increasethe IC mass effect and this may be avoided byadministration of steroids and early surgery afterthe procedure.46,59–61 Shunting of the embolicmaterial through the tumor in the setting of patent

pericytoma in the middle cranial fossa. (A) Axial; (B)

Fig. 29. There is marked vascular supply to lesion from two main branches arising from the internal maxillaryartery and left occipital artery (A, B). Figure C is during the embolization procedure.

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formane ovale may permit paradoxic embolizationto occur systemically. A hypertensive responsedue to release of vasoactive peptides from largechemodectomas may occur and cause death.This can be avoided by careful anesthetic prepara-tion and management.

Case Examples of Tumor Embolization

Patient 1: convexity meningioma withexternal carotid artery embolizationA 51-year-old woman presented with recenthistory of progressive headaches and memoryproblems. Neuroimaging demonstrated a largeparafalcine meningioma, causing significantmass effect over the right frontal lobes. Thetumor extended bilaterally across the superiorsagittal sinus occluding it midway in its course.The patient underwent cerebral angiogram onthe day before the operation and selective embo-lization of frontal division of the middle meningeal

artery supplying the tumor was done with 150 to250 PVA particles through a 4F Renegade witha gold-tip microcatheter (Target Therapeutics/Boston Scientific) under careful negative road-map observation until stasis of flow wasobserved. She underwent a craniotomy and totalresection of the tumor on the next day. Patientmade a smooth recovery.

Patient 2: clival meningioma withmeningohypohyseal trunk embolizationA 51-year-old woman presented with intractableseizure and on neuroimaging was found to haverecurrence of petroclival meningioma. On angiog-raphy, there were feeders from bilateral MHT, rightMMA, and distal IMA. Particle embolization wasperformed using a combination of 45- to 150-mmPVA particles in the right MHT and 150- to250-mm PVA particles in the internal maxillarybranches using a 6-Fr Marathon 1.3-Fr microcath-eter . There was significant reduction in the tumor

Fig. 30. There is vascular supply to the skull base lesion from branches of the inferolateral trunk and tumor vesselsoriginating near the MHT. There is a prominent posterior communicating artery infundibulum. After emboliza-tion of the ILT and MHT vessels, the tumoral flush was significantly reduced (not shown)

Fig. 31. (A) Coronal gadolinium MRI showing a contrast enhancing right mastoid mass lesion up to 4.1 cm in size.(B) CT with bone windows showing significant bone erosion.

481

Fig. 32. Angiography revealed on right carotid injection a prominent tumor stain corresponding to the knownright mastoid tumor. Early venous drainage is present and suggestive of arteriovenous shunt within the tumor.The tumor angiographic appearance suggests intraosseous meningioma.

Sekhar et al482

blush after the procedure and she underwentsurgical resection of the tumor.

Patient 3: recurrent hemangiopericytomawith embolizationA 58-year-old man with recurrent hemangiopericy-toma who underwent multiple resections andgamma knife radiosurgery for his tumor was sub-jected to balloon occlusion test and embolizationof tumor subsequently. In two sessions,

Fig. 33. Endovascular catheterization and embolization oraphy in the external carotid system demonstrated near-c

embolization was done. The 6-Fr Envoy catheterwas placed into the left ECA and an Excelsior 10microcatheter (eV3) with the assistance of Synchro14 microwire was advanced into an anterior andposterior division of the left internal maxillary arteryand occipital artery supplying the tumor, and PVAparticle embolization was carefully performedusing 150- to 250-mm particles and negative road-map technique. A large area of irregular tumorblush within the left aspect of the skull base

f the tumor using Onyx-18. (A) Postinjection angiog-omplete devascularization of the tumor (B).

Fig. 34. (A) Postembolization CT scan shows presence of Onyx in the mastoid tumor and (B) post gadolinium axialMRI shows Onyx with central necrosis of the tumor.


supplied by branches of the ILT and vessels nearthe MHT from the left ICA and AICA were also em-bolized. After particle embolization of the said ECAand ICA branches, there was stasis of flow withinthese vessels and markedly decreased tumorblush.

Patient 4: tumor with Onyx embolizationA 62-year-old woman presented with history ofheadaches and was discovered to have a large hy-pervascular tumor. She had a previous surgery forMeniere’s disease. Preoperative CT scan demon-strated significant bony erosion. MRI demon-strated multiple vascular flow voids. Angiographydemonstrated the mastoid tumor as extremelyvascular with prominent blush. Early venousdrainage was suggestive of arteriovenous shuntwithin the tumor. The tumor was embolized usingOnyx-18, PVA, and Gelfoam pledgets/torpedoesbefore surgery to reduce the extent of bleedingand reduce CN morbidity.

Results and Complications

At the authors’ institution over the last 3.5 years,18 convexity tumors, 42 skull base lesions, 19intrinsic brain tumors, and 23 EC neoplasmswere embolized by the endovascular team. Suchembolization often, but not always, resulted inthe reduction of bleeding during surgery andenhanced the ease of removal. There were nomajor complications encountered in the authors’experience.

SUMMARY

Endovascular procedures are rapidly expandingas treatment options for cerebrovascular diseasesand neoplasms of the head and neck and arebecoming less invasive but more effective. Thereare potentially dangerous anastomoses betweenthe EC and IC circulations; hence, thoroughknowledge of the anatomy is essential to minimizethe risk of CN palsies, blindness, or neurologicdeficits. It is essential to understand the scientificbasis of treatment rationale based on advancingnew neuroimaging techniques to better servepatients. An interdisciplinary approach and treat-ment in high volume centers are vital to obtainmaximal benefit for patients.

REFERENCES

1. Dawbain RH. The starvation operation for malignancy

in the external carotid area. JAMA 1904;17:792–5.

2. Macpherson P. The value of preoperative emboliza-

tion of meningioma estimated subjectively and

objectively. Neuroradiology 1991;33:334–7.

3. Manelfe C, Lasjaunias P, Ruscalleda J. Preoperative

embolization of intracranial meningiomas. AJNR Am

J Neuroradiol 1986;7:963–72.

4. Martin NA, Khanna R, Doberstein C, et al. Thera-

peutic embolization of arteriovenous malformations:

the case for and against. Clin Neurosurg 2000;46:

295–318.

5. Lundqvist C, Wikholm G, Svendsen P. Embolization

of cerebral arteriovenous malformations: part II—

aspects of complications and late outcome. Neuro-

surgery 1996;39:460–9.

Sekhar et al484

6. Weber W, Kis B, Siekmann R, et al. Endovascular

treatment of intracranial arteriovenous malformations

with onyx: technical aspects. AJNR Am J Neurora-

diol 2007;28:371–7.

7. Spetzler RF, Martin NA, Carter LP, et al. Surgical

management of large AVM’s by staged embolization

and operative excision. J Neurosurg 1987;67:17–28.

8. Vinuela F, Dion JE, Duckwiler G, et al. Combined endo-

vascular embolization and surgery in the management

of cerebral arteriovenous malformations: experience

with 101 cases. J Neurosurg 1991;75:856–64.

9. Gobin YP, Laurent A, Merienne L, et al. Treatment of

brain arteriovenous malformations by embolization

and radiosurgery. J Neurosurg 1996;85:19–28.

10. Henkes H, Nahser HC, Berg-Dammer E, et al. Endo-

vascular therapy of brain AVMs prior to radiosur-

gery. Neurol Res 1998;20:479–92.

11. Dawson RC 3d, Tarr RW, Hecht ST, et al. Treatment of

arteriovenous malformations of the brain with

combined embolization and stereotactic radiosurgery:

results after 1 and 2 years. AJNR 1990;11:857–64.

12. Dion JE, Mathis JM. Cranial arteriovenous malforma-

tions. The role of embolization and stereotactic

surgery. Neurosurg Clin N Am 1994;5(3):459–74.

13. Ogilvy CS, Stieg PE, Awad I, et al. Special Writing

Group of the Stroke Council, American Stroke Asso-

ciation. AHA scientific statement: recommendations

for the management of intracranial arteriovenous

malformations: a statement for healthcare profes-

sionals from a special writing group of the Stroke

Council, American Stroke Association. Stroke 2001;

32:1458–71.

14. Ondra SL, Troupp H, George ED, et al. The natural

history of symptomatic arteriovenous malformations

of the brain: a 24-year follow-up assessment. J Neu-

rosurg 1990;73:387–91.

15. Hernesniemi JA, Dashti R, Juvela S, et al. Natural

history of brain arteriovenous malformations:

a long-term follow-up Study of risk of hemorrhage

in 238 patients. Neurosurgery 2008;63:823–31.

16. Spetzler RF, Martin NA. A proposed grading system

for arteriovenous malformations. J Neurosurg 1986;

65(4):476–83.

17. Kim LJ, Albuquerque FC, Spetzler RF, et al. Postem-

bolization neurological deficits in cerebral arteriove-

nous malformations: stratification by arteriovenous

malformation grade. Neurosurgery 2006;59(1):53–9

[discussion: 53–9].

18. Hartmann A, Pile-Spellman J, Stapf C, et al. Risk of

endovascular treatment of brain arteriovenous mal-

formations. Stroke 2002;33(7):1816–20.

19. Steiner L, Lindquist C, Adler J. Clinical outcome of

radiosurgery for cerebral arteriovenous malforma-

tions. J Neurosurg 1992;77:1–8.

20. Valavanis A, Christoforidis G. Endovascular

management of cerebral arteriovenous malforma-

tions. Neurointerventionist 1999;1:34–40.

21. Natarajan SK, Ghodke B, Britz GW, et al. Multimo-

dality treatment of brain arteriovenous malforma-

tions with microsurgery after embolization with

onyx: single-center experience and technical

nuances. Neurosurgery 2008;62:1213–26.

22. Velat GJ, Reavey-Cantwell JF, Sistrom C, et al.

Comparison of N-butyl cyanoacrylate and onyx for

the embolization of intracranial arteriovenous malfor-

mations: analysis of fluoroscopy and procedure

times. Neurosurgery 2008;63(1 Suppl 1):ONS73–8

[discussion: ONS78–80].

23. Newton TH, Cronqvist S. Involvement of dural

arteries in intracranial arteriovenous malformations.

Radiology 1969;93:1071–8.

24. Sarma D, ter Brugge K. Management of intracranial

dural arteriovenous shunts in adults. Eur J Radiol

2003;46:206–20.

25. Cognard C, Houdart E, Casasco AE, et al. Endovas-

cular therapy and long term results for intracranial du-

ral arteriovenous fistulae. In: Connors JJ, Wojak JC,

editors. Interventional neuroradiology. 1st edition.

Philadelphia: Saunders Company; 1999. p. 198–214.

26. Graeh D, Dolman C. Radiological and pathological

aspects of dural arteriovenous fistulas. J Neurosurg

1986;64:962–7.

27. Watanabe A, Takahara Y, Ibuchi Y, et al. Two cases

of dural arteriovenous malformation occurring after

intracranial surgery. Neuroradiology 1984;26:

375–80.

28. Chaudhary M, Sachdev V, Cho S. Dural arteriove-

nous malformations of the major venous sinuses:

an acquired lesion. AJNR Am J Neuroradiol 1982;

3:13–9.

29. Kwon BJ, Han MH, Kang HS, et al. MR imaging

features of intracranial dural arteriovenous fistulas:

relations with venous drainage patterns. AJNR Am


30. Uranishi R, Nakase H, Sakaki T. Expression of angio-

genetic growth factors in dural arteriovenous fistula.

J Neurosurg 1999;91:781–6.

31. Lasjaunias P, Berenstein A, ter Brugge KG. Surgical

Neuroangiography. 2nd edition. Springer; 2001.

32. Awad IA, Little RJ, Akrawi WP, Ahl J. Intracranial dural

arteriovenous malformations: factors predisposing to

an aggressive neurological course. J Neurosurg

1990;72:839–50.

33. Lasjaunias P, Chiu M, terBrugge KT. Neurological

manifestations of intracranial dural sinus arteriove-

nous malformations. J Neurosurg 1986;64:724–30.

34. Cognard C, Gobin YP, Pierot L, et al. Cerebral dural

arteriovenous fistulas: clinical and angiographic

correlation with a revised classification of venous

drainage. Radiology 1995;194:671–80.

35. Brown RD Jr, Wiebers DO, Nichols DA. Intracranial

dural arteriovenous fistulae: angiographic predictors

of intracranial hemorrhage and clinical outcome in

nonsurgical patients. J Neurosurg 1994;81:531–8.


36. Halbach VV, Higashida RT, Hieshima GB, et al. Dural

fistulas involving the cavernous sinus: results of treat-

ment in 30 patients. Radiology 1987;163:437–42.

37. van Dijk JM, terBrugge KG, Willinsky RA, et al. Clin-

ical course of cranial dural arteriovenous fistulas

with long-term persistent cortical venous reflux.

Stroke 2002;33:1233–6.

38. Duffau H, Lopes M, Janosevic V, et al. Early rebleed-

ing from intracranial dural arteriovenous fistulas:

report of 20 cases and review of the literature. J

Neurosurg 1999;90:78–84.

39. Ushikoshi S, Houkin K, Kuroda S, et al. Surgical

treatment of intracranial dural arteriovenous fistulas.

Surg Neurol 2002;57:253–61.

40. Collice M, D’Aliberti G, Arena O, et al. Surgical treat-

ment of intracranial dural arteriovenous fistulae: role

of venous drainage. Neurosurgery 2000;47:56–66

[discussion: 66–7].

41. Caragine LP Jr, Halbach VV, Dowd CF, et al. Intraor-

bital arteriovenous fistulae of the ophthalmic veins

treated by transvenous endovascular occlusion:

technical case report. Neurosurgery 2006;58(Suppl

1):ONS-E170 [discussion: ONS-E170].

42. Koebbe CJ, Singhal D, Sheehan J, et al. Radiosur-

gery for dural arteriovenous fistulas. Surg Neurol

2005;64:392–9.

43. Soderman M, Edner G, Ericson K, et al. Gamma

knife surgery for dural arteriovenous shunts: 25

years of experience. J Neurosurg 2006;104:867–75.

44. American Society of Interventional and Therapeutic

Neuroradiology. Head, neck, and brain tumor embo-

lization. AJNR Am J Neuroradiol 2001;22:S14–5.

45. Hekster RE, Matricali B, Luyendijk W. Presurgical trans-

femoral catheter embolization to reduce operative

blood loss. Technical note. JNeurosurg 1974;41:396–8.

46. Chun JY, McDermott MW, Lamborn KR, et al.

Delayed surgical resection reduces intraoperative

blood loss for embolized meningiomas. Neurosur-

gery 2002;50:1231–7.

47. Ahuja A, Gibbons KJ. Endovascular therapy of

central nervous system tumors. Neurosurg Clin

N Am 1994;5:541–54.

48. Sekhar LN, Pomeranz S, Janecka IP, et al. Temporal

bone neoplasms: a report on 20 surgically treated

cases. J Neurosurg 1992;76:578–87.

49. Accreditation Council on Graduate Medical Educa-

tion. Carotid artery balloon test occlusion. AJNR

Am J Neuroradiol 2001;22(Suppl):S8–9.

50. Berdick TR, Hoffer EK, Kooy T, et al. Which arteries

are expendable? The practice and pitfalls of embo-

lization throughout the body. Semin Intervent Radiol

2008;25:191–203.

51. Qureshi AI. Endovascular treatment of cerebrovas-

cular diseases and intracranial neoplasms. Lancet

2004;363:804–13.

52. Lapresle J, Lasjaunias P. Cranial nerve ischaemic

arterial syndromes. A review. Brain 1986;109(Pt 1):

207–16.

53. Lasjaunias P, Doyon D. The ascending pharyngeal

artery and the blood supply of the lower cranial

nerves. J Neuroradiol 1978;5(4):287–301.

54. Robinson DH, Song JK, Eskridge JM. Embolization

of meningohypophyseal and inferolateral branches

of the cavernous internal carotid artery. AJNR Am


55. George B, Casasco A, Deffrennes D, et al. Intratu-

moral embolization of intracranial and extracranial

tumors: technical note. Neurosurgery 1994;35:

771–3 [discussion: 773–4].

56. Casasco A, Herbreteau D, Houdart E, et al. Devas-

cularization of craniofacial tumors by percutaneous

tumor puncture. AJNR Am J Neuroradiol 1994;15:

1233–9.

57. Chaloupka JC, Mangla S, Huddle DC, et al. Evolving

experience with direct puncture therapeutic emboli-

zation for adjunctive and palliative management of

head and neck hypervascular neoplasms. Laryngo-

scope 1999;109(11):1864–72.

58. Kallmes DF, Evans AJ, Kaptain GJ, et al. Hemor-

rhagic complications in embolization of a menin-

gioma: case report and review of the literature.

Neuroradiology 1997;39:877–80.

59. Gruber A, Killer M, Mazal P, et al. Preoperative

embolization of intracranial meningiomas: a 17-

year single center experience. Minim Invasive Neu-

rosurg 2000;43:18–29.

60. Adler JR, Upton J, Wallman J, et al. Management

and prevention of necrosis of the scalp after embo-

lization and surgery for meningioma. Surg Neurol

1986;25:357–60.

61. Halbach VV, Hieshima GB, Higashida RT, et al. Endo-

vascular therapy of head and neck tumors. In:

Vinuela F, Halbach VV, Dion JE, editors. Interventional

neuroradiology: endovascular therapy of the central

nervous system. New York: Raven Press; 1992. p.

17–28.

neuroendovascular management of tumors and vascular malformations of the head and neck

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