AJNR Am J Neuroradiol 25:1131-1138, August 2004

Neurophysiologic Monitoring and PharmacologicProvocative Testing for Embolization of Spinal

Cord Arteriovenous Malformations

Yasunari Niimi, Francesco Sara, Vedran Deletis, Avi Sellon,Adauri Bueno de Camargo, and Alex Berenstein

BACKGROUND AND PURPOSE: Embolization of a spinal cord arteriovenous malformation(SCAVM) is still considered risky. We evaluated the efficacy and reliability of pharmacologicprovocative testing with neurophysiologic monitoring in the embolization of SCAVMs.

METHODS: We retrospectively analyzed results of 60 provocative tests during 84 angiographicprocedures (in 52 patients) with intended endovascular embolization. Tests included 47 sodiumamytal and 56 lidocaine injections. All procedures were performed with general anesthesia andmonitoring of cortical somatosensory evoked potentials (SEPs) and trans cranial motor evokedpotentials (MEPs). For provocative testing, 50 mg of amytal and 40 mg of lidocaine were consec-utively injected through a microcatheter placed at the position of intended embolization. If SEPsand MEPs did not change, embolization was performed with N-butyl-cyanoacrylate(NBCA).If SEPsor MEPs changed, NBCA embolization was not performed from that catheter position.

RESULTS: One false-negative result occurred, with an increase in spasticity after emboliza-tion. Nineteen positive results occurred: four after amytal injection and 15 after lidocaineinjections. Seven injections in a posterior spinal artery feeder resulted in loss of SEPs or MEPs.Eleven injections in the anterior spinal artery feeder and one in the posterior inferior cerebellarartery feeder resulted in loss of MEPs.

CONCLUSION: Provocative testing with amytal and lidocaine combined with neurophysio-logic monitoring had a high negative predictive value and was a useful adjunct for SCAVMembolization. Both amytal and lidocaine should be used as provocative agents, and both SEPsand MEPs should be monitored.

Although embolization is now accepted as a usefultreatment option for spinal cord arteriovenous mal-formations (SCAVMs), it is still considered a high-risk procedure because of the potential for spinalcord ischemia. To avoid neurologic complications, theblood supply to the normal spinal cord should bepreserved during embolization. For this purpose, it isessential to superselectively catheterize the nidus ofthe malformation and to carefully analyze the vascu-lar anatomy. Because of small and overlapping nor-

Received July 7, 2003; accepted after revision January 5, 2004.From the Center for Endovascular Surgery (Y.N., AS., AB.)

and Division of Intraoperative Neurophysiology (v.D., AB.d.c.),Hyman Newman Institute for Neurology and Neurosurgery, BethIsrael Medical Center Singer Division, New York, NY, and theSection of Neurosurgery, Department of Neurological Sciencesand Vision, Verona University, Italy (F.S.).

Address reprint requests to Yasunari Niimi, MD, Center forEndovascular Surgery, Hyman Newman Institute for Neurologyand Neurosurgery, Beth Israel Medical Center Singer Division, 170East End Avenue at 87th Street, New York, NY 10128.

mal and pathologic vessels, the vascular supply of thespinal cord can be difficult to identify in cases ofSCAVM, despite the use of magnification or addi-tional lateral and oblique angiograms. Furthermore,because of the hemodynamic changes caused by theSCAVM, the normal spinal cord supply might not bepredictable with angiographic findings alone.

In addition to careful angiographic analysis, phar-macologic provocative testing is used to identify thefunctional eloquence of the territory of a catheterizedvessel. This testing is usually performed by clinicallyassessing the patient's neurologic status after the in-jection a short-acting anesthetic via a microcatheterplaced in a feeding artery before embolization (1).This method requires the patient to be awake. How-ever, for spinal cord embolization procedures, weprefer to use general anesthesia to control the pa-tient's breathing to obtain high-resolution images.This helps us to identify the small spinal cord vesselsand enhances the patient's comfort during this po-tentially long procedure. To assess the patient's1__'- -,-,--. __.L"- L- -- .L. ,. "-- 1

1132 NIIMI

anesthesia, we have used neurophysiologic moni-toring during pharmacologic provocative testing.

We initially started by monitoring only cortical so-matosensory evoked potentials (SEPs) (2), but theirreliability in assessing the corticospinal tract was notideal (3). Therefore, we added motor evoked poten-tials (MEPs) to the SEPs. One of major problems ofprevious MEP-monitoring techniques was its inva-siveness, with the need to place recording electrodesthrough a burr hole to elicit MEPs and to use epi-durally inserted electrodes to record them (4). One ofthe present authors (V.D.) has established a protocolfor a noninvasive technique of trans cranial corticalstimulation, along with recording from peripheralmuscles (5-8). Our preliminary data for this tech-nique were published (9). Since then, our experienceand understanding of neurophysiologic monitoringhas increased substantially. We retrospectively re-viewed our data and changed our interpretation ofprovocative test results from positive to negative inone case. (In this case, SEPs were thought to be lostafter an injection of lidocaine into the anterior spinalartery [ASA] feeder, but this result was a fluctuationof the electrical response most likely related to thedepth of anesthesia.) The purpose of this study was toupdate our experience with SCAVM embolization byusing this monitoring technique. To our knowledge,this is the first large series of SCAVMs embolized byusing SEP and MEP monitoring and pharmacologicprovocative testing.

Methods

Since 1996, 52 patients with SCAVMs underwent 84 spinalcord angiographic procedures. Endovascular embolization wasperformed in the same setting as the angiography wheneverfeasible. During these procedures, 60 provocative tests wereperformed. The results of SEP and MEP monitoring, provoc-ative tests, and embolization were retrospectively analyzed.

During angiographic assessment and embolization, the pa-tients were given general anesthesia by means of a continuousinfusion of propofol (100-150 J.Lglkg/min) and fentanyl (1 J.Lg/kg/h). After anesthesia was induced, no inhalational anestheticswere used.

SEP and MEP Monitoring

SEP monitoring was performed in a conventional method(10). Briefly, SEPs were elicited by stimulating the right andleft posterior tibial nerves at the ankle and the median nervesat the wrist with electric stimuli (40 mA, 0.2-ms duration,4.3-Hz repetition rate). SEPs were recorded via corkscrew-typeelectrodes (Spinal Corkskrew Electrode; Nicolet, Madison,WI) placed on the patient's scalp over the primary sensorycortex. MEPs were elicited with transcranial electrical stimula-tion of the motor cortex by using corkscrew type electrodes(Nicolet). Short trains of 5-7 square-wave stimuli of 500-J.Lsduration and 4-milIisecond interstimulus intervals were appliedat a I-Hz repetition rate through electrodes placed at Cl andC2 scalp sites according to the International 10/20 EEG Sys-tem. The intensity of stimulation did not exceed 200 IDA.Muscle responses were recorded with needle electrodes in-serted in the bilateral anterior tibialis, toe abductor, and thenarmuscles. Recordings from the upper-extremity muscles wereused as controls (6) for embolization of thoracic or lumbar

-.

AJNR: 25, August 2004

SEPs and MEPs were recorded at the beginning of theprocedure as the baseline after the induction of general anes-thesia and then immediately before provocative testing andembolization. The monitorability of SEPs and MEPs was as-sessed by the number of the monitorable limbs below the levelof the malformation. For example, if monitorable MEPs wereobtained from only the left upper and lower extremities in apatient with a cervicalSCAVM, the monitorability of the MEPswas 2 of 4. If monitorable MEPs were obtained from a1\fourextremities in a patient with a thoracic SCAVM, the monitor-ability was 2 of 2. When the lesion involved the conus of thespinal cord, we also monitored bulbocavernosus reflexes(BCRs). These oligosynaptic reflexes a1\owedus to assess thefunctional integrity of both afferent and efferent fibers of thepudendal nerves, as we1\as the reflex center located in the graymatter at the S2-S4 spinal levels. The technical details aredescribed elsewhere (11, 12).

Provocative TestingProvocative testing was performed just before the injection

of a liquid embolic agent for embolization of a1\ nidus-typearteriovenous malformations (AVMs) and arteriovenous fistu-las (AVFs) when there was some distance between the tip ofthe microcatheter and the fistula site. Provocative testing wasnot performed for an extradural component of the malforma-tion or if the tip of the microcatheter was close to the fistula siteof an AVF. Provocative testing was also not performed beforeparticle or coil embolization. Superselective digital subtractionangiography was performed to study the normal and abnormalvascular anatomy with the microcatheter placed as close aspossible to the AVM at the location intended for embolization.Contrast material was injected under roadmap fluoroscopy todetermine the optimal force for injection to distribute theanesthetic distal enough without creating reflux near the mi-crocatheter tip. This was fo1\owedby provocative testing forneuronal function with an intra-arterial injection of 50 mg ofsodium amytal. If SEPs or MEPs did not change, 20-40 mg oflidocaine was injected intra-arteria1\y depending on the feedersize and degree of shunting. If SEPs or MEPs stilI did notchange, embolization was performed by using N-butylcyanoac-rylate (NBCA) from that catheter position. If the amplitude ofSEPs decreased by >50% or if MEPs disappeared after theinjection of amytal or lidocaine, the result was consideredpositive, and NBCA embolization from that position was notperformed. If amytal produced a positive result, the test wasconsidered positive and lidocaine was not injected. If the lido-caine test was positive after a negative amytal test, a secondprovocative test in the same vascular territory was performedby injecting only lidocaine, after we advanced the microcath-eter further dista1\yor protected the normal territory with aliquid coil.Technical details are described elsewhere (8, 12). Incases of a radicular feeder to the vascular malformation, pro-vocative testing was performed with monitoring of the MEPs ofthe related nerve distribution. For example, deltoid and bicepsMEPs were monitored for provocative testing in the C5 radic-ular feeder.

Results

SEP and MEP Monitoring

SEP and MEP monitoring was attempted in all 84procedures. Embolization was performed in 48. In 36procedures, no feasible feeder was available for em-bolization, or embolization was attempted and aborted,because it was impossible to perform catheterizationdistal enough to consider embolization, or becauseprovocative test results were positive. MonitorableC'DDn n.~_~ ~h'n;~=r1 ;~ c:.c:. 1:;01- (1 1:;-::),~f ')-::).(\ l;~ho\ "",.1

AJNR: 25, August 2004 SPINAL CORD ARTERIOVENOUS MALFORMATION 1133

TABLE 1: Summary of provocative test results

Sodium Amy tal

No. of Positive ResultsVessel No. of Vessels

ASAPSAPosterior inferior cerebellar arteryRadicular arteryTotal

321311

47

31004

TABLE 2: Summary of positive provocative test results

* MEPs and SEPs were monitored from only one leg because of

previous amputation of the other leg.

MEPs in 83.9% (198 of 230 limbs). BCRs were moni-torable in 76.7% of attempted cases (66 of 86 sides in43 patients). Sixty provocative tests were performed,with 19 positive results (31.7%). Forty-seven amytaltests were performed, with four (8.5%) positive re-sults. Fifty-six lidocaine tests were performed, with 15(26.8%) positive results (Table 1). Table 2 summa-rizes the positive results.

A positive amytal result occurred after one injec-tion in the posterior spinal artery (PSA) and twoinjections in the ASA feeders, resulting in loss ofMEPs. In one patient with a conus AVM, bilateralBCRs and MEPs were lost without changes in SEPsafter an injection of amytal into the ASA feeder. Thepositive lidocaine results involved six injections in thePSA (loss of MEP in two, SEPs in one, MEPs andBCRs in two, and MEPs and SEPs in one), eightinjections in the ASA (loss of MEPs in eight), and oneinjection in the posterior inferior cerebellar arterywith loss of MEPs. Once a positive result was ob-tained with an injection of amytal, lidocaine was notinjected from the same microcatheter position. Onlyone injection of an anesthetic (amytal or lidocaine)resulted in the loss of both MEPs and SEPs. Eachpositive test resulted in either unilateral or bilateralloss of MEPs or SEPs. Whether unilateral or bilateralresponses would be lost were not predictable basedon findings of superselective angiography performedwith the microcatheter. In one patient, the injectionof lidocaine into an ASA feeder of the cervical<;;:r A '\Tl\Jf re>cn lte>r! ;,.., the> tr",..,o;e>,..,t r!;o"nn""rcon('" of

MEPs from both upper extremities without changesin lower-extremity MEPs.

Provocative Testing

After positive provocative testing and disappear-ance of MEPs or SEPs, MEPs or SEPs recovered tothe baseline value within 15 minutes for the initialtesting in all patients. Recovery of MEPs or SEPstended to be delayed up to 1 hour after the second orthird injection of amytal or lidocaine in the samepatient. This was the notable limiting factor for re-peating a provocative test. No patient underwentmore than three sets of provocative tests during oneangiography and embolization session.

Of 19 patients with positive provocative test results,embolization was aborted in six.Two patients of thesepatients had two consecutive positive results on re-peated provocative tests, as assessed by advancing amicrocatheter distally. Embolization with NBCA waspossible in five patients by further advancing a micro-catheter. One patient previously had two consecutivepositive results during microcatheter advancement.One patient underwent embolization with dilutedparticles, and another patient received coils. In onepatient, we performed a clinical provocative test tofurther clarify a positive provocative test result byusing electrophysiologic monitoring. We woke thepatient from general anesthesia, injected the samepharmacologic agent (lidocaine), and assessed thepatient for new neurologic signs. We thought that thiswake-up test was indicated in this young patient withprogressive neurologic deterioration, because wewere able to achieve an optimal catheter position forembolization, and NBCA embolization was believedto be safe. This patient underwent embolization withNBCA after the wake-up test showed no changes inneurologic signs. In one patient, a positive result wasdue to the reflux of lidocaine to the ASA, which hada common origin with the PSA feeder. This patientunderwent embolization with gentle antegrade NBCAinjection without reflux. In one patient, a normalPSA was found by advancing the microcatheter.NBCA embolization was performed after we pro-tected the normal territory with liquid injectablemicro coils (Table 3). Details of this procedure arereported elsewhere (13).

Only one patient had worsening of symptoms afterthe embolization, as shown on the results of the pro-"o(',:,t;"". t,,«!>: Th;« n,:,t;p.nt h,:,rJ ~ tr~n!':ip.nt wor!,:p.ninlJ

Lidocaine

No. of Vessels No. of Positive Results

37 815 6 '"1 13 0

56 15

No. ofProcedures

Agent and Vessel Change (n = 19)

Sodium amy talPSA Unilateral MEP 1ASA Unilateral MEP 2ASA Bilateral BCR, unilateral MEP 1*

LidocainePSA Bilateral MEP 1PSA Bilateral MEP and SEP 1PSA Unilateral MEP 1PSA Unilateral SEP 1

PSA Unilateral MEP and BCR 2ASA Unilateral MEP 4ASA Bilateral MEP 4PICA Unilateral MEP 1

1134 NIIMI

TABLE 3: Actions taken after positive provocative test results

Action No.

Aborted embolizationAdvanced catheter and embolization with NBCA

Distal vessel protection and embolization with NBCAEmbolization with particlesEmbolization with coils

Embolization with NBCA after negative wake-up test

Embolization with NBCA with less forceful injection

6'st11111

* In two patients, the procedure was aborted after two consecutive

positive results during advancement of a microcatheter.t In one patient, embolization was performed by advancing a mi-

crocatheter from the proximal positions where two positive results wereobtained.

of spasticity after NBCA embolization through anASA feeder after a negative provocative test.

Illustrative Cases

Patient 1.-A 24-year-old woman initially pre-sented with progressive weakness and numbness ofthe right lower extremity since the age of 17 years. At23 years old, she had a spinal subarachnoid hemor-rhage. Spinal angiography demonstrated a SCAVMthat extended from C5 to C7 (Fig lA). She underwenttwo previous endovascular embolization proceduresfor this SCAVM, with partial occlusion of the nidus.During the second procedure, the ASA feeder wasembolized from the dorsocervical artery, with sub-stantially decreased opacification of the nidus andpreservation of the ASA axis (Fig lB). At the time ofthe third procedure, spontaneous thrombosis and dis-connection of the ASA axis were discovered (Fig Ie).The ASA was superselectively catheterized to theorigin of this remaining feeder, and digital subtrac-tion angiography was performed (Fig ID). Whetherthis vessel provided collateral supply to the normalspinal cord at the level of the occluded ASA segmentwas unclear on angiograms. On the basis of the neg-ative provocative test result, this was embolized withNBCA (Fig IE), without aggravating the patient'sneurologic conditions.

Patient 2.-A 20-year-old man had a cervicalSCAVM that extended from C5 to C6. He initiallypresented with cervical subarachnoid hemorrhage atthe age of 10years and underwent three embolizationprocedures to decrease the size of the nidus. He laterdeveloped a small hematomyelia without neurologicdeterioration. Follow-up angiograms demonstrated aremaining cervical SCAVM supplied by the ASA andthe lateral spinal artery from the vertebral artery andalso the ASA from the dorsocervical artery (Fig 2A).After embolization from the ASA through the verte-bral artery, the feeder from the radiculomedullaryartery from the dorsocervical artery was superselec-tively catheterized. Superselective angiography dem-onstrated a feeder on the surface of the spinal cordsupplying the malformation (Fig 2B-D). It was notpossible to determine if this vessel supplied the func-.' 1 ___'__1 J -- .1..- 1 '- ~& --_:~ 1..:- &, j

AJNR: 25, August 2004

ings. Because the lidocaine injection from the micro-catheter caused both upper-extremity MEPs todisappear, we decided not to embolize this feeder.

Discussion

In the early 1980s, we started monitoring SEPsduring spinal cord angiography and embolization,with relatively good reliability (2, 14). Later, severalreports noted that SEP monitoring failed to predictpostoperative motor deficits (3, 15). Although bothSEP and MEP monitoring is frequently used in spinalcord surgery, MEP monitoring during embolization isnot often used because of its invasiveness (eg, burr-hole placement for eliciting MEPs and inserting epi-dural electrodes for recording them) (4). One of thepresent authors (V.D.) established our protocol forreliable and noninvasive MEP monitoring in the mid-1990s (7, 8). We now routinely use SEP and MEPmonitoring in all spinal angiography procedures withintended embolization, including cases of SCAVMs,spinal dural AVFs, and spinal tumors. This monitor-ing is useful for the early detection of ischemia due toblocked flow in the spinal cord artery from vaso-spasm, the microcatheter, or the effects of particleembolization. One of the illustrative cases demon-strating the high sensitivity of SEP and MEP moni-toring was previously reported (7). Monitorable SEPsand MEPs can be obtained, even in patients withexisting moderate sensory or motor deficits. However,monitorab1e SEPs often cannot be obtained in pa-tients who have lost proprioception. In addition, SEPsand MEPs are sensitive to the depth of anesthesia,even without the use of muscle relaxants or inhala-tional anesthetics. Therefore, it is important to obtainbaseline recordings just before provocative testing isdone. For thoracic and lumbar lesions, upper-extrem-ity responses can be used as controls. For conus le-sions, we also monitor BCRs. Absent BCRs are wellcorrelated with symptoms of bladder, bowel, or sexualdysfunction. The clinical use of BCR monitoring forspine and spinal cord embolization is still underinvestigation.

Regarding pharmacologic provocative testing, alow dose of a short-acting barbiturate, such as amytal,predominantly suppresses neuronal activity (16) asopposed to a low dose of lidocaine, which predomi-nantly suppresses axonal conduction in the CNS (17).Therefore, both agents should theoretically be usedfor better reliability of provocative testing. However,we do not inject lidocaine when we have a positiveresult with amytal, because it does not change theinterpretation of the already-positive result. In ourseries, lidocaine caused more positive results than didamytal. The most likely reason is that lidocaine blocksnerve transmissions through the fibers traversing theanesthetized area, as opposed to amytal, which blockstransmission of neurons in the anesthetized area. Themotor pathway affected by amytal may not be detect-able because of a limited number of muscles moni-tored with the MEP technique. Therefore, we have

j...j~...j ~~-;.~-;-~ ~+ ;~~~_'n_' ~no~lp<. ;n o..",,~;n~

4

AJNR: 25, August 2004 SPINAL CORD ARTERIOVENOUS MALFORMATION 1135

c

D

F

FIG 1. Illustrative patient 1.A, Anteroposterior (AP) view of the right dorsocervical artery obtained before embolization shows a large AVM involving C5-C7 and

supplied by the ASA.B, AP right dorsocervical angiogram obtained after second embolization shows decreased opacification of the nidus with preservation

of the anterior spinal axis (arrowheads) with one remaining indirect feeder (arrows).C, AP right dorsocervical angiogram obtained 11 months after second embolization at the time of third embolization shows

spontaneous occlusion of the anterior spinal axis (arrowhead) and the remaining indirect feeder (arrow). Note the decreased caliber ofthe ASA proximally and the increased diameter of the indirect supply. Compare with B.

D, AP superselective ASA angiogram from just before the origin of the feeder shows complete occlusion of the anterior spinal axisdistal to this origin. Arrowhead indicates the microcatheter tip in the anterior spinal axis. Arrows indicate the remaining feeder. Becauseprovocative test results were negative, we embolized the malformation from this position with NBCA; symptoms did not worsen.

E, AP right vertebral angiogram after third embolization. ASA is opacified from above, with minimal supply to the remaining nidus(arrowhead) mainly supplied by the vertebral artery branch. There is slow flow in the radiculomedullary artery from the right dorsocervicalartery (arrow), which reaches the level of embolization in a later phase (not shown).

F, Schematic illustration of the AVM in relation to the spinal cord. A indicates vertebral artery; B, radiculomedullary artery from thedorsocervical artery; C, ASA; D, feeders embolized in the first two procedures; E, feeder embolized in the third procedure; F, AVM nidus;and G, ASA segment occluded in the third embolization.

cases, such as diaphragmatic MEPs for lesions in thehigh cervical cord. For radicular feeders to a malfor-mation, we place additional electrodes to monitorl\tfPP~ from mll~('lp~ ~llnnlipr1 nv thp nf'.rvf'. Toot ~t the

level of the lesion. Although we have not yet hadpositive results from the provocative testing withthese additional MEPs, the number of patients issmall. and further investilration is needed.

1136 NIIMI AJNR: 25, August 2004

c

B

E

In our series, one injection of amytal and five in-jections of lidocaine in the PSA resulted in the loss ofMEPs. In contrast, changes in SEPs occurred in onlytwo injections in the PSA, one of which resulted inchanges in both MEPs and SEPs. All positive resultsfrom amytal or lidocaine injections in the ASA causeda loss of MEPs without changes in SEPs. Althoughthe ASA is generally thought to supply the anterolat-eral motor pathways and the PSA supplies the poste-rior sensory pathways of proprioception, our obser-vation suggests that the superselective injection ofanesthetics through the PSA can affect motor path-ways. This effect may be due to the rich anastomosisbetween ASA and PSA branches, especially in thepresence of an AVM. There may also be a hemody-namic shift of the watershed zone between the ASAand the PSA territories due to the presence of theAVM nr nrpvinm: f'.mhnli7:1tinn Amnnp- six nMients

FIG 2. Illustrative patient 2.A, AP right dorsocervical angiogram demon-

strates a pial feeder (arrow) to the AVM origi-nating from the radiculomedullary artery justbefore the origin of the anterior spinal axis.

B-O, AP (B and C) and lateral (D)superselec-tive angiograms of the radiculomedullary feederin early (B) and late (C and D) phases. Arrowindicates microcatheter tip. The malformation isdraining to the anterior spinal vein (arrow-heads). This was not embolized, because pos-itive provocative test results indicated supply tothe normal spinal cord.

E, Schematic shows the AVMin relation tothe spinal cord. A indicates radiculomedullaryartery; B, pial feeder; C, ASA;and 0, AVMnidus.

in whom MEPs were lost with provocative testingfrom a PSA feeder, four had supply from both theASA and PSA. One patient had supply to the AVMfrom the contralateral PSA across the midline, andanother patient had a common trunk between theASA and the PSA. In four patients, angiogramsshowed rich anastomoses between the ASA and PSA,and two patients had undergone a previous emboli-zation procedure. Although SEPs did not change inany patients after anesthetics were injected in theASA, this occurred in our experience (2, 14). Whenwe first started electrophysiologic monitoring, we in-jected only amytal as a provocative agent and wereable to monitor only SEPs during provocative testing(1, 2). At that time, we avoided complications ofembolization due to false-negative provocative resultsby more frequently performing the wake-up test (ie,reneatim! the orovocative test bv temoorarilv awak-

AJNR: 25, August 2004 SPINAL CORD ARTERIOVENOUS MALFORMATION 1137

ening the patient and injecting amytal to evaluateclinical changes). However, waking the patient andre-inducing general anesthesia was cumbersome anduncomfortable for the patient, and interpretation ofthe results was sometimes difficult because the pa-tient was too sleepy during testing. Our data suggestthat both SEPs and MEPs should be monitored re-gardless of whether the provocative test is performedin the ASA or PSA.

The 'negative predictive value of our provocativetest was high (97.6%), even when we considered onecase of transiently increased spasticity after emboli-zation as a false-negative finding. With the currenttechnique of MEP monitoring, subtle changes (eg,increased spasticity without worsening of motorstrength) cannot be reliably predicted. If results of aprovocative test are negative, however, the malforma-tion might be safely embolized from that catheterposition by using a liquid embolic agent without caus-ing damage. In patient 1, deciding to embolize thisfeeder with a liquid agent would have been difficult ifprovocative testing liad not been available. On thebasis of our previous experience, we could comfort-ably embolize this feeder with NBCA because of thenegative provocative test result.

A positive provocative test result generally indi-cates normal supply to the spinal cord downstream ofthe tip of the microcatheter. In patient 2, this ASAbranch might have been embolized if we had notperformed provocative testing, because this feederwas a pial branch and did not originate from the ASAaxis itself. The positive result suggested that this ves-sel might supply the motor pathway to both upperextremities; therefore, embolization of this vesselwith NBCA was aborted. However, the number oftrue-positive and false-positive results is unknown,because we generally do not embolize the malforma-tion with a liquid agent from that catheter position ifthe provocative test result is positive. Therefore, thesensitivity, specificity, accuracy, and positive predic-tive value cannot be calculated; this is a limitation ofthis type of clinical study. We had only one false-positive result, which occurred in a cervical SCAVM;in this case, an injection of lidocaine caused the rightlower-extremity MEPs to disappear. Because the po-sition of the micro catheter was thought to be suitablefor NBCA embolization, the patient was awakened,and the lidocaine test was repeated. The second in-jection did not cause worsening of motor strength,and the AVM was embolized from this catheter positionwith a liquid agent without worsening of symptoms.

Theoretically, false-positive results can occur be-cause the distribution pattern of the liquid embolicmaterial differs from that of anesthetics; this reflectsthe different viscosities and injection forces, as well asthe progressively polymerizing nature of the embolicmaterial as opposed to persistently liquid nature ofanesthetics. False-negative results can also happenfor the same reasons, but these are rare in our expe-rience. These may be owing to the relatively largedoses of amytal (50 mg) and lidocaine (40 mg) used to

,',' H,", "_L.1LLL__u' d-

eter tip, as well as the tendency of the embolic agentto penetrate less than amytal or lidocaine because ofits higher viscosity and progressively polymerizing na-ture. Therefore, we think that this method of provoc-ative testing tends to overestimate the risk of embo-lization, resulting in its high negative predictive value.

A provocative test result that is positive indicatesan increased risk of functionally damaging the spinalcord during embolization with liquid material fromthat catheter position. The best solution is to advancethe microcatheter closer to the nidus and repeat pro-vocative testing. If the second result is negative, em-bolization can be performed with a liquid agent. An-other solution is to protect the normal territory byusing a fiber or liquid coil. If, after blocking thenormal territory, the repeat result is negative, liquidembolization can be performed (13). If neither ofthese solutions is possible, embolization might still beperformed by using particles, depending on the flowdynamics in the feeder. If none of these alternatives ispossible, embolization from another feeder should beconsidered. In a patient in whom embolization ishighly indicated but results of provocative testing atthe best catheter position are positive, a wake-up testmay be considered if angiography indicates a goodcatheter position for embolization. However, per-forming liquid embolization despite a positive resultviolates the safety margin of the provocative testingbecause of its tendency to overestimate the risk ofembolization. Therefore, this decision should bemade carefully on the basis of precise angiographicanalysis and the indication for embolization. If we areconfident that liquid embolization can be performedsafely from a certain catheter position (eg, microcath-eter tip in the venous side of a fistula), provocativetesting is not necessary. We performed less provoca-tive testing for fistulous malformations than for ni-dus-type malformations. In cases with previous inter-ventions and altered anatomy, testing is of greatvalue.

Provocative testing with amytal and lidocaine, andmonitoring of MEPs and SEPs are useful adjuncts toSCAVM embolization under general anesthesia andmake the procedure safer and more comfortable forthe operator. However, this testing should not replacecareful angiographic analysis of the vascular anatomy.

Neurophysiologic monitoring during embolizationof brain AVMs is also performed in a small numberof cases in our institution. However, we need moreclinical experience and technical refinement to estab-lish a reliable method. For example, transcranial elec-trical stimulation of the motor cortex to elicit muscleMEPs directly stimulates the subcortical axons of themotor pathways; this might cause false-negative pro-vocative test results for cortical lesions. Deep anes-thesia completely blocks trans-synaptic activation ofthe fast neurons of the corticospinal tract, whichmakes stimulation of the gray matter of the motorcortex unreliable. Multiple electrodes can obstructangiographic visualization of the detailed vascularanatomy, even when a subtraction technique is used.T:'..-1__'__- "- .1-.-.1-._1_~..0-..r1 1-._0_1~_..~1;- l\,fPP

1138 NIIMI

and SEP monitoring should help in predicting themotor and sensory functional outcome of emboliza-tion. For brain stem lesions, monitoring of MEPs,SEPs, and brain stem auditory evoked potentials, withMEPs from cranial nerve-innervated muscles (eg,facial and glossopharyngeal nerves [corticobulbartract]), may provide sufficient safety information be-fore embolization.

Conclusion

Neurophysiologic provocative testing with amytaland lidocaine is a useful adjunct to SCAVM emboli-zation under general anesthesia. Both MEPs andSEPs should be monitored whether provocative test-ing is performed in the ASA or PSA. If the result isnegative, the AVM can be comfortably embolized byusing a liquid embolic agent. If it is positive, aggres-sive embolization with a liquid agent poses a high riskof spinal cord damage. The decision should be basedon careful angiographic analysis of the malformationand the indication fot treatment.

References

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