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Epilepsy Research (2013) xxx, xxx—xxx

jou rn al h om epa ge: www.elsev ier .com/ locate /ep i lepsyres

REVIEW

The utility of ambulatory electroencephalography inroutine clinical practice: A critical review

Udaya Seneviratnea,b,∗, Armin Mohamedc, Mark Cooka, Wendyl D’Souzaa,d

a Department of Medicine, St. Vincent’s Hospital, University of Melbourne, Victoria Parade, Fitzroy 3065, Australiab Department of Neuroscience, Monash University & Monash Medical Centre, Clayton 3168, Melbourne, Australiac Comprehensive Epilepsy Service, Royal Prince Alfred Hospital & The University of Sydney, Camperdown, Sydney, NSW 2050,Australiad Centre for Molecular, Environmental, Genetic & Analytic Epidemiology, Melbourne School of Population Health, University ofMelbourne, Australia

Received 14 August 2012; received in revised form 19 December 2012; accepted 11 February 2013

KEYWORDSAmbulatory EEG;Long-termmonitoring;Epilepsy

Summary Over the last four decades, ambulatory electroencephalography (EEG) has evolvedto be a useful tool in the diagnosis of epilepsy and certain nonepileptic paroxysmal disorders.Most of the initial technological drawbacks of ambulatory EEG have been circumvented byincorporating digital and computer technology. It appears superior to routine EEG in capturinginterictal abnormalities particularly in relation to natural sleep, circadian variations and the

patient’s typical daily lifestyle. The role of ambulatory EEG in studying seizures and nonepilepticparoxysmal events remains to be defined by targeted research. It perhaps is an underutilizedtool and more research is needed to expand the horizon of ambulatory EEG applications inclinical practice. Crown Copyright © 2013 Published by Elsevier B.V. All rights reserved.

Contents

Introduction............................................................................................................... 00The evolution of ambulatory EEG: a historical perspective ................................................................ 00Technical challenges ...................................................................................................... 00

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

Artifacts...................................................Data storage...............................................Battery life................................................

∗ Corresponding author at: Department of Neuroscience, St. Vincent’s

Tel.: +61 03 9288 3341; fax: +61 03 9288 3350.E-mail addresses: udaya.seneviratne@svhm.org.au, udaya.seneviratn

0920-1211/$ — see front matter. Crown Copyright © 2013 Published by Ehttp://dx.doi.org/10.1016/j.eplepsyres.2013.02.004

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

........................................................... 00

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Hospital, PO Box 2900, Fitzroy VIC 3065, Melbourne, Australia.

e@monash.edu (U. Seneviratne).

lsevier B.V. All rights reserved.

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Clinical applications....................................................................................................... 00Diagnosis of epilepsy and epilepsy syndromes......................................................................... 00

Studies with ≤8 channels in adult and mixed-age populations.................................................. 00Studies with ≤8 channels in pediatric populations ............................................................. 00Studies with ≥16 channels in adult and mixed-age populations ................................................ 00Studies with ≥16 channels in pediatric populations ............................................................ 00

Diagnosis of nonepileptic paroxysmal disorders ....................................................................... 00Assessment of treatment: response and antiepileptic withdrawal..................................................... 00Evaluation for epilepsy surgery ....................................................................................... 00

Strengths of ambulatory EEG .............................................................................................. 00Cost .................................................................................................................. 00Convenience.......................................................................................................... 00Capturing natural sleep and circadian variations...................................................................... 00Yield ................................................................................................................. 00

Limitations of ambulatory EEG ............................................................................................ 00Interpretation of clinical events ...................................................................................... 00AED tapering ......................................................................................................... 00Technical limitations ................................................................................................. 00Cosmetic issues....................................................................................................... 00

Practical recommendations on outpatient ambulatory EEG without video recording ....................................... 00The choice of ambulatory EEG vs. VEM ............................................................................... 00

Indications ................................................................................................ 00Diagnosis and classification of epilepsy ........................................................................ 00Correlation of epileptiform discharges with behavioral consequences.......................................... 00Quantification ................................................................................................. 00Assessment of subclinical seizure activity...................................................................... 00

Assessment of response to therapy, AED withdrawal and occupational safety including fitness to drive.... 00Cautions .................................................................................................. 00

Characterization of behavioral events ......................................................................... 00Recognition of epileptiform abnormalities ..................................................................... 00

Presurgical evaluation in refractory epilepsy .............................................................. 00Technical aspects..................................................................................................... 00

Behavioral monitoring..................................................................................... 00Self reporting.................................................................................................. 00

Observer reporting........................................................................................ 00Duration of monitoring ............................................................................................... 00Safety ................................................................................................................ 00

Conclusions and future directions ......................................................................................... 00Conflict of interest ........................................................................................................ 00Funding sources ........................................................................................................... 00References ................................................................................................................ 00

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mbulatory electroencephalography (ambulatory EEG) hasmerged as a cost-effective alternative for inpatient video-lectroencephalographic monitoring (VEM) in the diagnosisf epilepsy and other paroxysmal disorders. It offers thedvantage of continuous EEG monitoring in the real life sett-ngs, which may be more convenient and acceptable to theatient. The technology of ambulatory EEG has come a longay from 4-channel, analog tape recorders to 32-channel,igital, computer-assisted devices. Ambulatory EEG can beerformed in both the inpatient and outpatient settings

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

ith maximum mobility of the subject (Cascino, 2002).ynchronous video recording may or may not be availableepending on the system. In this review, we confine ouriscussion to outpatient ambulatory EEG. We provide an

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verview of the evolution of ambulatory EEG technology andts applications, followed by an analysis of published studiesn clinical applications and practical recommendations.

he evolution of ambulatory EEG: a historicalerspective

he concept of continuous electrophysiologic monitoring inmbulatory patients came to limelight with Holter’s inven-ion of a portable recorder of electrocardiography (ECG)Holter, 1961). In 1972, a 4-channel device for continuous

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

ecording of physiological signals became available (Marsonnd McKinnon, 1972). Three years later, the clinical applica-ion of that technology in the form of ambulatory EEG wasescribed (Ives, 1975). The device consisted of four channels

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with a portable cassette recorder capable of data storage forover 24 h, worn over the shoulder or around the waist. Thepreamplifier pack had to be taped onto the patient’s neckand then connected to the recorder by a cable. The nextmajor breakthrough was the invention of a miniature pream-plifier attachable to the scalp with collodion (Quy, 1978). In4-channel devices, EEG montages were designed to utilizethree of the channels and the fourth was usually used as atimer, event marker, or ECG recorder (Bridgers and Ebersole,1985).

In the early 1980s, an 8-channel ambulatory EEG sys-tem with digital time and event markers was introduced.Cassette tapes were still in use for data recording. The incor-poration of off-head preamplifiers was a major step forward(Ebersole, 1985). In the late 1980s, 16-channel ambulatoryEEG was introduced by linking two cassette recorders.

In the 1990s, digital technology was incorporated intoambulatory EEG (Gilliam et al., 1999). The number of chan-nels was increased up to 32. Removable hard drives wereused for storage initially. Subsequently, the advent of flashmemory technology made it possible to record and store EEGcontinuously for 24 h or more. Computer-assisted spike andseizure detection programs were introduced with a view toincreasing the efficiency of reviewing the large amount ofdata acquired through continuous EEG monitoring (Gotman,1982). However, to date, visual analysis by an expert remainsthe gold standard.

Discontinuous or epoch recording was introduced as a wayof storing selected EEG data over a longer period. The firstdevice was introduced in 1982. The recorder saved epochs atregular intervals and in relation to push-button activationswith events. Later, with the incorporation of computer tech-nology, spike and seizure detection programs were used toselect and save abnormal segments (Ebersole et al., 2003).However, with the advent of smaller digital storage deviceswith increased capacity, the need for discontinuous recor-ding has become obsolete.

The incorporation of synchronized digital video recordingto ambulatory EEG has greatly enhanced the interpreta-tion of clinical events captured. This has been achievedwith the use of a video camera with a wide-angle lens con-nected to a computer via a cable and synchronized with EEG(Schomer et al., 1999). This ambulatory EEG system can beset up at the patient’s home. Though it compromises mobil-ity compared to traditional ambulatory EEG without videorecording, this system is likely to be preferred over inpa-tient VEM by patients. Current ambulatory EEG systems arecommercially available in two forms; with and without videorecording. However, the system with video is the preferredchoice due to its advantage in providing visual phenomeno-logical details.

Technical challenges

Artifacts

In comparison to inpatient VEM, ambulatory EEG without

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video recording poses a challenge in differentiating betweenartifacts and epileptiform abnormalities. Electrode, muscleand movement artifacts are major challenges in ambula-tory EEG recordings due to its unsupervised nature. With

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raditional EEG electrodes, a conductive gel connects thelectrode to the scalp. When the gel dries up, the elec-rode becomes loose and the impedance increases makingay to artifacts. In the inpatient setting this problem isircumvented by regular relubricating of electrodes. Thiss not possible with ambulatory EEG and the patient usuallyisits the EEG laboratory once a day for the readjustment oflectrodes, which can be problematic for patients who haveo travel long distance. Certain daily activities produceovement artifacts which might resemble epileptiform dis-

harges (Fig. 1). On the other hand, epileptiform dischargesan be masked by muscle and movement artifacts.

There are several potential approaches to overcome thisroblem. Patients and carers could be trained to relubri-ate the electrodes. Some ambulatory EEG systems providehe option of remote online access to assess the qualityf EEG recording and take remedial action (Casson et al.,010). Some researchers have envisaged that dry electrodesnd semi-implanted electrodes (subcutaneous and subder-al) could solve this problem in future (Casson et al., 2010).ry electrodes do not require special preparation or lubri-ant gel, hence are more user friendly. The technology inhis area is evolving (Fonseca et al., 2007). The feasibilityf the use of subdermal electrodes in long-term continu-us EEG monitoring has been demonstrated in the intensiveare unit setting (Martz et al., 2009). However, the possibil-ty of infection remains a potential problem with long-termonitoring.

ata storage

he flash memory technology has revolutionized data stor-ge. The quantity of data acquired through ambulatory EEGepends on the sampling rate, resolution, number of chan-els and length of recording. The incorporation of videoecording would also increase the amount of data stored.ost of the current ambulatory EEG systems can store data

n the memory card up to 72 h at 256 Hz sampling rateith 12 bit resolution for 26—32 channels. Compression algo-

ithms are used for online data transmission.

attery life

attery life is a major rate-limiting step in the currentmbulatory EEG systems. Some machines use recharge-ble batteries, which however heavily depend on patientompliance. Battery changing by the EEG technologist onegular basis is an alternative. Researchers have proposed tomprove the electronic design in order to reduce the poweronsumption thus extending the battery life (Casson et al.,010).

linical applications

iagnosis of epilepsy and epilepsy syndromes

nterictal epileptiform abnormalities on the EEG aid epilepsy

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

iagnosis and syndromic classification. However, the yieldepends on several internal and external factors includinghe length, timing with respect to sleep—wake cycle and theechnique of recording (Seneviratne et al., 2012). Among

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atients with epilepsy, the routine EEG demonstrates epilep-iform abnormalities in 40—55% of recordings, and the yieldncreases to 80—90% with sleep deprivation and repeatedecordings (Goodin and Aminoff, 1984; Leach et al., 2006;arsan and Zivin, 1970; Salinsky et al., 1987). Recording theEG within two days of a seizure also appears to increase theield (68%) (Sundaram et al., 1990). However, it is difficulto extrapolate these results into routine clinical practiceue to heterogeneity of study populations and methodology.

Ambulatory EEG offers the advantage of a long recordncluding natural sleep and typical lifestyle in capturing bothnterictal epileptiform discharges (IED) and seizures. Com-arison between ambulatory EEG studies is difficult due toeterogeneity as illustrated in Table 1. We have made anttempt to summarize the findings based on the number ofhannels used for recording and the age distribution.

tudies with ≤8 channels in adult and mixed-ageopulations

n a retrospective analysis of 500 patients who underwentmbulatory EEG, IED were detected in 11% whilst seizuresere captured on 6.5% of recordings (Bridgers and Ebersole,985). The total yield of seizures and IED were higher inhe subgroup of patients referred by neurologists (20.4%)nd in those who were referred with a suspected diagnosisf a seizure disorder (34.9%), indicating that the yield mayepend on the pre-test probability of the patient populationtudied. After performing routine EEGs in the same cohort,he researchers found a 21-fold increase in seizure yield and1% increase in IED yield with ambulatory EEG (Bridgers andbersole, 1985). It should be noted that only three EEG chan-els were used in both adults and children with recordingengths ranging from 6 h to 24 h. Another study reported clin-

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

cal events in 86% (epileptic 54%, nonepileptic 32%) (Oxleynd Roberts, 1985).

The yield of 4-channel ambulatory EEG was comparedith routine EEG in a cross-over study. Ambulatory EEG

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troencephalography recording. Note the muscle and movement

as recorded for 24 h whilst the mean duration of routineEG was 17 min with hyperventilation and photic stimulationCull, 1985). A modest increase in focal IED (9.7% vs. 6.5%)nd generalized IED (21% vs. 12.9%) was found on ambula-ory EEG, though statistical significance was not specified.his is discordant with the higher yield reported in othertudies cited above. A plausible explanation is masking ofpileptiform paroxysms by frequent muscle and movementrtifacts as declared by the authors.

On comparison between three and eight-channel ambu-atory EEG systems, the latter was found to be superiorn differentiating epileptiform abnormalities from arti-acts and normal transients, thus reducing false positivesEbersole and Bridgers, 1985).

When 3-channel ambulatory EEG was compared with rou-ine EEG and inpatient cable EEG telemetry (CEEG) in aohort of 40 patients, 37% of ambulatory EEG and 44% ofEEG recordings detected epileptiform abnormalities whenhe routine EEG was normal. In comparison to CEEG, 79%f focal IED, 100% of generalized IED and 100% of seizuresere concordant on ambulatory EEG (Ebersole and Leroy,983). CEEG used montages based on eight channels with

better spatial resolution than 3-channel ambulatory EEG,hich could be the reason for lower yield of focal IED onmbulatory EEG. All the captured seizures were either gen-ralized or complex partial. Ambulatory EEG was as good asEEG in detecting those seizures despite having fewer chan-els, most probably due to widespread electric field of theeizures.

tudies with ≤8 channels in pediatric populations retrospective audit found epileptiform electrographicbnormalities in 50% of ambulatory EEGs, in comparison to

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

3% of routine EEGs performed in children. Clinical eventsere captured in 31 patients (57%), out of which only threead epileptic seizures (Saravanan et al., 2001). Increasedength of recording (minimum 48 h) and patient selection

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U.,

et al.,

The utility

of am

bulatory electroencephalography

in routine

clinical practice:

A critical

review.

Epilepsy Res.

(2013), http://dx.doi.org/10.1016/j.eplepsyres.2013.02.004

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Table 1 Comparison of studies on ambulatory electroencephalography.

Reference Design Total Age range(mean)years

Indications fortest/cohortcharacteristics

Video used Recordinglength (h)

Number ofchannels

Yield IED Yieldseizures

Yield NEE

Aminoff et al.(1988)

NS 95 0.5—16 (1) Clinicallydefinite epilepsy,(2) ‘‘spells’’ ofuncertain etiology

No 24 4 NS 55% 44%

Bridgers andEbersole (1985)

R 500 0.2—82 Suspected epilepsyand NEE

No 6—24 4 11% 6.5% 15.4%

Chang et al. (2002) R 7 22—43 Presurgical workupfor refractorytemporal lobeepilepsy

No 5—21 days ≥16 NS 100% —

Cull (1985) NS 62 13—81(35.3)

Episodes of loss ofconsciousness

No 24 4 30.7% NS 6.5%

Dash et al. (2012) P 101 13—60(36.6)

Differentiatebetween seizuresand NEE, diagnoseepilepsy, quantifyseizure activity,characterize seizuretype and location

No 15—96 24 NS NS 30.8%

Ebersole andLeroy (1983)

NS 40 NS Epilepsy No 16—24 4 60% 17.5% —

Faulkner et al.(2012b)

R 324 12—79 (39) Diagnosis andclassification ofepilepsy andnonepilepticattacks, diagnosis ofsubclinical seizures

No 72—96 32 36% 17% 30%

Foley et al. (2000) R 84 1.5—18 (1) Diagnosed or (2)suspected epilepsy

No 1—4 days 18 NS 45% and17% 43% and 69%

Koepp et al.(2008)

P 15 22—85 For AED withdrawalin patients seizurefree ≥3 years

No 24 16 40% NS NS

Lai and Ziegler(1981)

CR 1 NS Episodes of loss ofconsciousness

No NS 4 0 0 Asystole

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bulatory electroencephalography

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A critical

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Epilepsy Res.

(2013), http://dx.doi.org/10.1016/j.eplepsyres.2013.02.004

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Table 1 (Continued)

Reference Design Total Age range(mean)years

Indications fortest/cohortcharacteristics

Video used Recordinglength (h)

Number ofchannels

Yield IED Yieldseizures

Yield NEE

Liporace et al.(1998)

P 46 NS Diagnostic study forepilepsy

No 24 16 33% 15% NS

Morris et al. (1994) R 344 0.5—69 NS No Average 32 16 26.2% 11.9% 36.3%Olson (2001) R 167 0.3—18 (7.2) Diagnosis of

epilepsy vs. NEE,diagnosis ofsubclinical seizures,localizing seizureonset

No Average1.9 days

16 NS 20.4% 68%

Oxley and Roberts(1985)

R 100 16—50 Diagnosis ofepilepsy vs. NEE,diagnosis ofsubclinical seizures,localizing seizureonset

No 48—216 4 NS 54% 32%

Saravanan et al.(2001)

R 54 1—16 (10.2) Diagnosis ofepilepsy vs. NEE

No 48 8 50% 5.5% 18.5%

Schomer et al.(1999)

CR 1 28 Presurgical workupfor refractorytemporal lobeepilepsy

No ≥24 16 many many —

Tatum et al.(2001)

R 502 0.8—93(35.3)

Diagnosis ofepilepsy

No Mean 28.5 16 NS 8.5% NS

Wang et al. (2011) R 214 7—38 For AED withdrawalin patients seizurefree ≥3 years

No 24 16 20.1% NS NS

Wirrell et al.(2008)

P 64 ≤17 Diagnosis ofepilepsy vs. NEE,classification ofseizure type,determineseizure/IEDfrequency

No Mean 32.7 16 78% 28% 78%

AED: antiepileptic drugs; CR: case report; IED: interictal epileptiform discharges; NEE: nonepileptic events; NS: not specified; P: prospective; R: retrospective.

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criteria (clinical events happening at least once in 24 h onmost days/nights and age) may account for this higher yield.However, syndromes are not specified in the paper.

Another study reported a very high seizure yield of 55%(Aminoff et al., 1988). A selected sample of children diag-nosed with clinically definite epilepsy was studied and 17.5%of them had already shown electrographic seizures on rou-tine EEG. Hence, the high yield is most probably due toselection criteria employed.

Studies with ≥16 channels in adult and mixed-agepopulationsA retrospective study based on 16-channel, computer-assisted, ambulatory EEG involving 344 patients recordedIED in 26.2% and seizures in 11.9% (Morris et al., 1994).Both figures are higher than those reported by Bridgers andEbersole (1985), which could be explained on the basis ofhigher number of channels used (16 vs. 4) and longer recor-ding duration. The average recording length was 32 h whilstages ranged from 6 months to 69 years. 95% of the refer-rals were from neurologists, but the proportion of differentepilepsy syndromes and the indications for ambulatory EEGwere not specified. On subgroup analysis of ambulatory EEGdata when the routine EEG was normal or non-specific, theauthors found a modest decrease in the yield (seizures 6.8%,IED 25.1%) compared to the total cohort, though no statisti-cal inferences were made.

In a cohort of patients with a suspected diagnosis ofepilepsy and normal routine EEG, both sleep-deprived EEGand 16 channel-ambulatory EEG increased the yield of IED(24% and 33%, respectively, difference not statistically sig-nificant). Seizures were captured in 15% of ambulatory EEGrecordings compared to none in sleep-deprived EEG. Inter-estingly, patients were aware of only 50% of the seizures asindicated by push-button activation (Liporace et al., 1998).

Poor self awareness of seizures among patients withepilepsy has been well described. A study from a video EEGlaboratory found that 63% of seizures were not rememberedby patients. Secondarily generalized tonic-clonic seizureswere more likely to be missed compared to primary general-ized tonic-clonic seizures and non-generalized focal seizures(Blum et al., 1996). This phenomenon was further eval-uated with ambulatory EEG using push-button activationto indicate subjects’ awareness of seizures. It was foundthat 38.3% of seizures were unreported by patients (Tatumet al., 2001). Concordant findings (33%) were reported fromanother study using similar methodology (Olson, 2001). Theresults indicate that ambulatory EEG can be used to diagnoseunrecognized seizures, which has potential implications onmanagement including assessment of fitness to drive.

In a recent study where prolonged (96 h), continuousambulatory EEG was recorded with a 26 channel system,the median latency to the first IED was found to be 316 min.IEDs were recorded in 95% within 48 h. The latency to thefirst IED was significantly shorter in generalized epilepsiescompared to focal epilepsies (Faulkner et al., 2012a). Thisstudy demonstrates the value of ambulatory EEG in the diag-nosis and classification of epilepsies as the routine EEG has

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

a lower yield and sensitivity.In another study from Australia, based on 96-h ambula-

tory EEG recordings, yields for IED and epileptic seizureswere found to be 36% and 17%, respectively. Overall, the

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mbulatory EEG helped change the management in 51%Faulkner et al., 2012b).

A recent study reported that ambulatory EEG contributedo confirming the diagnosis in 71% of patients. The testielded useful information on the diagnosis of epilepsy anduantification of epileptiform discharges as well as seizuresn 25%. Ambulatory EEG was well tolerated and a client satis-action questionnaire revealed a high degree of satisfactionith the test (Dash et al., 2012).

tudies with ≥16 channels in pediatric populations very high yield of IED (78%) and seizures (28%) waseported in a prospective study involving children (Wirrellt al., 2008). The sampling bias may account for this find-ng. All patients were referred by pediatric neurologists formbulatory EEG as an alternative for inpatient VEM for char-cterization of clinical events and estimation of seizure/IEDrequency. Furthermore, 81% of prior routine EEG had shownED indicating this was a very selective cohort.

The value of computer-assisted outpatient EEG in captur-ng seizures among children and adolescents was evaluatedetrospectively in a study (Foley et al., 2000). Subjects wereivided into two groups; group 1: patients diagnosed withpilepsy by a neurologist and referred due to unresponsive-ess of habitual events to antiepileptic drugs (AED), novelymptoms or discrepancy between abundance of IED in rou-ine EEG and reported seizure frequency, group 2: patientsith suspected epilepsy (Foley et al., 2000). In group 1,abitual events were captured in 88%, comprising seizuresn 45% and nonepileptic events in 43%, whereas in group 2he yields were 86%, 17% and 69%, respectively. These find-ngs suggest that the yield may depend on patient selectionriteria.

In a retrospective study of 167 children who under-ent ambulatory EEG, clinical events were recorded in9% (nonepileptic 68%, epileptic 20.4%, mixed 0.6%) (Olson,001). This yield is concordant with group 2 of Foley et al.2000) study.

Magnetoencephalography (MEG) has emerged as an alter-ative diagnostic tool to detect interictal epileptiformischarges (IED). In a retrospective study, the yield of IEDn MEG (60%) and simultaneous EEG/MEG (71%) were higherhan the yield in sleep-deprived EEG (51%) though the dif-erence was not statistically significant (Heers et al., 2010).nother study has drawn similar conclusions (63% yield inEG vs. 57% in sleep-deprived EEG) (Colon et al., 2009).here are no studies available directly comparing ambula-ory EEG with MEG.

In general, all of these studies suggest that the yieldf ambulatory EEG depends on technical aspects, length ofecording and patient selection criteria. It appears superioro routine EEG in picking up both IED and seizures, thougho robust conclusions can be drawn with the available dataue to study heterogeneity and variable confounding factorsnvolved. There is insufficient data to compare ambulatoryEG with inpatient VEM.

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

iagnosis of nonepileptic paroxysmal disorders

mbulatory EEG could be a useful diagnostic tool to dif-erentiate epileptic seizures from nonepileptic paroxysmal

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vents such as psychogenic nonepileptic seizures, syncopend some sleep disorders. The incorporation of additionalhannels for ECG, electromyography, and pulse oximetrynto ambulatory EEG systems has enhanced this capability.ince the invention of 4-channel ambulatory EEG, an ECGhannel has been in routine use helping identification ofardiogenic paroxysmal events. Push-button event markersnd event diaries are useful for EEG correlation with clin-cal events. The lack of simultaneous video recording is aajor drawback in the interpretation of such events. There

re difficulties in differentiating nonepileptic events frompileptic seizures with certainty in the absence of simulta-eous video recording. This problem has been circumventedn some ambulatory EEG systems with the incorporation of

home computer-based digital video recording. Studies onhe use of ambulatory EEG in nonepileptic paroxysmal eventsre scant.

In a case report, ambulatory EEG/ECG established theiagnosis of cardiac asystole as the cause of recurrent lossf consciousness and seizure activity (Lai and Ziegler, 1981).

single case of symptomatic cardiac arrhythmia and sixases with features of narcolepsy were detected in a seriesf 500 patients who underwent ambulatory EEG. In the sametudy, only one had epileptiform EEG abnormalities from aubgroup of 67 subjects with symptoms of syncope, near-yncope or episodic dizziness (Bridgers and Ebersole, 1985).

Ambulatory EEG studies involving children and adoles-ents have reported capture rates of 78% (Wirrell et al.,008), and 76% (Olson, 2001) for nonepileptic events. Threeimilar studies reported lower yields of 53.6% (Foley et al.,000), 51.9% (Saravanan et al., 2001) and 44% (Aminofft al., 1988). The nature of nonepileptic events was notpecified in these studies. It should also be noted that nonef the studies used video recordings for detailed semiolog-cal analysis and the diagnosis was based on push-buttonctivation of events, absence of epileptic ictal rhythm onhe EEG, eye-witness descriptions as well as event diaries.his methodology is vulnerable for generating both falseositive and false negative results. Some epileptic seizures,articularly those of frontal lobe origin, may not be accom-anied by a visible ictal rhythm on scalp EEG (Williamson,992). Simple partial seizures as well as certain types of psy-hogenic nonepileptic seizures may not cause any changen the background EEG rhythm (Seneviratne et al., 2010).ome psychogenic nonepileptic seizures cause rhythmic EEGhanges due to movement artifact (Seneviratne et al.,010), which may be misinterpreted as an epileptic ictalhythm, particularly if not analyzed in conjunction withemiologic features. The recall of features of seizures byye-witnesses has been shown to be of low accuracy (Rugg-unn et al., 2001). Therefore, caution should be exercised

n interpreting results on nonepileptic events from ambula-ory EEG studies without concomitant video recordings foremiological analysis. However, the presence of a reactiveosterior rhythm during an attack of non responsiveness is

useful diagnostic clue for nonepileptic events. Some psy-hogenic nonepileptic seizures generate distinct EEG ictalhythms due to specific muscle and movement artifacts,

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

hich could be helpful in the diagnosis (Seneviratne et al.,010; Vinton et al., 2004).

Studies have demonstrated that about 10—13% of PNESopulation has coexistent epilepsy (Seneviratne et al.,

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010). Ambulatory EEG could be a valuable diagnostic tooln this category, when well-controlled patients with epilepsyubsequently present with an increase in seizure frequencynd apparent resistance to therapy due to emergence ofNES.

ssessment of treatment: response andntiepileptic withdrawal

raditionally, the response to various forms of therapy inpilepsy is measured by the seizure frequency reportedy patients. However, studies have shown that patientsay not be aware of up to 60% of their seizures, particu-

arly in sleep (Blum et al., 1996; Stefan and Hopfengartner,009). Outpatient ambulatory EEG has been proposed as

more reliable, objective method of measuring seizurerequency to evaluate response to therapy and the feasi-ility of this technique has been shown in patients withntractable epilepsy (Stefan et al., 2011). The same groupas demonstrated the practical value of outpatient ambu-atory video-EEG in assessing response to transcutaneousagus nerve stimulation in patients with pharmacoresistantpilepsy (Stefan et al., 2012).

The value of EEG in predicting the success of AED with-rawal is controversial. A meta-analysis found a high rate ofeizure relapse on AED withdrawal when the previous EEGad been abnormal (Berg and Shinnar, 1994). On the con-rary, in a large-scale, prospective, multicentre, randomizedtudy, the results were inconclusive (Medical Researchouncil Antiepileptic Drug Withdrawal Study Group, 1991).tudies on the use of ambulatory EEG in this regard arecarce.

In a small cohort of 15 adult patients with epilepsynd learning disability who had been seizure free (median0 years), all 6 patients who had IED on ambulatory EEGelapsed on AED withdrawal (Koepp et al., 2008). However,he sample is too small to draw a robust conclusion. Anothertudy involving 214 patients with epilepsy, who had beeneizure free for over 3 years, reported interictal abnormali-ies in 41.1% (IED in 20.1%, nonspecific abnormalities in 21%)n 24-h ambulatory EEG performed in the workup for AEDithdrawal (Wang et al., 2011). However, the outcome ofED withdrawal is not specified in the publication.

valuation for epilepsy surgery

n the literature, only two papers from the same centerave addressed this subject. Reviewing the topic, Schomert al. (1999) provide an example of a patient with refractoryemporal lobe epilepsy, who underwent successful temporalobectomy aided by outpatient ambulatory EEG monitor-ng. The same group published a series of seven patientsho had epilepsy surgery for temporal lobe epilepsy with

he help of outpatient ambulatory EEG. In comparison to aroup of patients with similar characteristics who underwentnpatient VEM, mean recording duration and the number of

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

eizures captured were less in ambulatory EEG though notatistical inferences were drawn (Chang et al., 2002). Dueo small sample size and retrospective design, it is diffi-ult to draw conclusions from this study regarding optimum

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Utility of ambulatory electroencephalography

patient selection criteria for ambulatory EEG in the presur-gical workup.

Even with concomitant video recording, ambulatory EEGis fraught with several practical limitations such as inabil-ity to taper AEDs due to safety concerns and the lack ofan assessment by an experienced observer during a seizure.Hence, the application of ambulatory EEG technology in thepresurgical evaluation appears to be limited in the currentcontext.

Strengths of ambulatory EEG

Cost

One of the main advantages of ambulatory EEG is lower costcompared to inpatient VEM. One study assessed the cost ofambulatory EEG to be 51—65% lower (Foley et al., 2000).In the Australian model, according to our estimates, inpa-tient VEEG monitoring is four times costlier than outpatientambulatory EEG, taking into account capital, staffing andconsumables (Faulkner et al., 2012b).

Convenience

Inpatient VEM is much more resource and labor inten-sive. Ambulatory EEG offers the option of continuous EEGmonitoring in the patient’s usual environment, which maybe more convenient and acceptable to some. We haveanecdotal examples of negative diagnostic inpatient VEMrecordings where ambulatory EEG was able to record typicalevents (unpublished data).

Capturing natural sleep and circadian variations

A major advantage of ambulatory EEG is its ability to capturenatural sleep and associated epileptiform abnormalities.Circadian variations of IED and seizures are well known(Seneviratne et al., 2012). A study based on ambulatoryEEG confirmed the phenomenon of epileptiform dischargeson awakening in idiopathic generalized epilepsy (Fittipaldiet al., 2001). In a cohort of adult epilepsy patients in clinicalremission, ambulatory EEG performed prior to AED with-drawal demonstrated IED in 40 all of whom relapsed. It isnoteworthy that 83% had IED exclusively in natural sleep(Koepp et al., 2008). Ambulatory EEG provides a great oppor-tunity to study IED and seizures associated with sleep andcircadian variations in different epilepsies which may haveimplications on the diagnosis and prognosis.

Yield

The value of EEG in the diagnosis and classification of epilep-sies is well established. Ambulatory EEG appears superior toroutine EEG in picking up both interictal and ictal epilep-tiform abnormalities, though the available data are notconclusive. It is potentially a very useful tool in the diag-

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

nosis and classification of epileptic disorders, particularlywhen the routine EEG is normal.

The yield of seizure recordings in ambulatory EEG com-pared to inpatient VEM is unclear. In a small study, the mean

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umber of seizures captured in ambulatory EEG was 7.4n comparison to 8.4 in inpatient VEM, though no statisti-al conclusions were made (Chang et al., 2002). On oneand, with AED tapering, inpatient VEM tends to record moreeizures (Marks et al., 1991). On the other hand, inpatienteizure frequency appears to be less than spontaneous habit-al frequency (Riley et al., 1981). Ambulatory EEG is a way ofapturing spontaneous seizures in the natural environment.ence, in medically refractory patients, it may be possibleo assess seizure frequency in patients’ own environment,sing ambulatory EEG without AED tapering. However, theresn’t sufficient data to draw any conclusions and more stud-es are needed to define the place of ambulatory EEG as aethod of seizure monitoring.

imitations of ambulatory EEG

n ILAE commission report has recommended that‘ambulatory outpatient and community based long-termonitoring may be used as a substitute for inpatient

ong-term monitoring in cases where the latter is not cost-ffective or feasible or when activation procedures aimedt increasing seizure yield are not indicated’’ (Velis et al.,007). There are several practical and technical limitationsf ambulatory EEG that should be taken into account in thenterpretation of data.

nterpretation of clinical events

he very nature of outpatient monitoring in ambulatoryEG comes with certain disadvantages. Examination of theatient during and after a seizure by an experienced per-on provides useful localizing and lateralizing information.his objective is hard to achieve outside the hospital set-ing. The lack of correlation between semiology and EEG is

major drawback unless video recording is incorporated. Inhe absence of a video, for clinical-EEG correlation one haso depend on push-button records and event diaries whichay not be very accurate. Hence, differentiating nonepilep-

ic events from epileptic seizures could be challenging.

ED tapering

apering of AEDs is routinely done in hospital-based VEMn order to increase the yield. One would anticipate greateluctance among clinicians for AED tapering in ambulatoryEG due to safety concerns (Velis et al., 2007).

echnical limitations

rtifacts are a concern when ambulatory EEG is conductedutside the hospital setting without the supervision of

technologist. Common artifacts in ambulatory EEG areaused by movements, muscle activity and poor electrodeontact. Differentiating those from epileptiform abnor-alities could sometimes be difficult without studying

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

ynchronous video recording. When ambulatory EEG is runor over 24 h, usually the patient has to visit the EEGaboratory everyday for adjustment and re-lubrication oflectrodes. Though, with improved technology, the current

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mbulatory EEG systems are capable of producing high-delity recordings (Foley et al., 2000), inability to takerompt action on faulty electrodes is a drawback.

Even when video recording is incorporated into ambula-ory EEG, the patient may move out of the camera’s rangeVelis et al., 2007). Inpatient VEM could continue underupervision until sufficient information is gathered. How-ver, the duration of outpatient ambulatory EEG is limitedy technical constraints as described.

osmetic issues

urrent ambulatory EEG systems are light and easy to carry.et, the electrodes need to be attached to the scalp. Evenhough it could be masked to an extent, some patients maynd it socially embarrassing outside the hospital.

ractical recommendations on outpatientmbulatory EEG without video recording

he American Clinical Neurophysiology Society and the ILAEave published guidelines on long-term EEG monitoringncluding some recommendations on ambulatory EEG (Velist al., 2007; American Clinical Neurophysiology Society,008). We have formulated practical suggestions based onhose two publications and our literature review. Thesehould only be considered preliminary and tentative rec-mmendations on outpatient ambulatory EEG, until moreomprehensive and authoritative guidelines are publishedy a professional body.

he choice of ambulatory EEG vs. VEM

utpatient ambulatory EEG may be a cost-effective alter-ative for inpatient VEM to capture IEDs/events in aaturalistic setting when seizure activation procedures areot deemed necessary.

ndications

iagnosis and classification of epilepsyutpatient ambulatory EEG may be considered in the appro-riate clinical setting, particularly when the routine EEG isnconclusive.

orrelation of epileptiform discharges with behavioralonsequencesithout synchronous video recording one has to depend on

he log maintained by the patient and an observer. It shoulde noted that such logs and diaries are less reliable thanideo recording. Hence, ambulatory EEG with synchronousideo is the preferred option.

uantificationmbulatory EEG can be used to measure the number, fre-

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

uency and duration of interictal and ictal epileptiformctivity as well as their temporal relationship to 24-h-cycle.t is also useful in the evaluation of circadian variations ineizure activity.

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PRESSU. Seneviratne et al.

ssessment of subclinical seizure activityt is known that patients may not be aware of some of theireizures. Ambulatory EEG can be used for qualitative anduantitative assessment of subclinical seizure activity byorrelating the EEG with patient’s seizure log.

ssessment of response to therapy, AED withdrawal andccupational safety including fitness to driveiven the advantage of ambulatory EEG in providing quan-ification and circadian variations of seizure activity, thesere potential indications though the evidence is thin atresent due to the lack of studies.

autions

haracterization of behavioral eventsEM is often performed to characterize various behavioralvents and correlate with EEG activity with a view tolassifying those events as epileptic or nonepileptic. Thisistinction could be difficult without detailed analysis ofemiology on the video. Hence, outpatient ambulatory EEGithout video is not the preferred investigation for this indi-ation.

ecognition of epileptiform abnormalitiesome artifacts might mask or resemble epileptiform EEGbnormalities. The differentiation can be difficult withoutynchronous video correlation.

resurgical evaluation in refractory epilepsyutpatient ambulatory EEG has major drawbacks such ashe lack of video for semiological analysis, inability toeduce AEDs due to safety concerns and the lack of super-ision/assessment by an experienced observer during aeizure. Hence, inpatient VEM is the preferred investigationor presurgical workup.

echnical aspects

isk electrodes should be applied with collodion. Periodicefilling with conductant gel to ensure optimum contacthould be done at least every 24 h. The impedance is bestept at or below 5000 �.

The ambulatory EEG system should have a minimum of6 EEG channels and storage capacity of at least 24 h of EEGata.

Single-channel electrocardiography (ECG) recordinghould be used with the EEG to detect cardiac conductionbnormalities which may be associated with clinical eventsn question and to correlate with ECG artifact on EEG.

The use of ‘‘event button’’ by the patient (or anbserver) to indicate clinical events (‘‘turns’’) is encour-ged.

ehavioral monitoring

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

elf reportinghe patient should be advised to keep a diary on theccurrence of events or ‘‘turns’’ in question. The time ofccurrence and detailed descriptions should be noted.

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Observer reportingDetailed documentation of clinical events by an observer,usually a family member or a friend, should be encouragedto supplement the patient’s seizure log. If possible, videorecording of clinical events (‘‘turns’’) by the observer shouldbe encouraged.

Duration of monitoring

This should be tailored to the individual patient depend-ing on several factors such as the indication, frequency ofclinical events, tolerability of the test and compliance. Ingeneral, 24—48 h of monitoring is usually well tolerated andoften provides sufficient information.

Safety

As outpatient ambulatory EEG is done without continuoussupervision by trained personnel, maximum safety precau-tions should be taken. Seizure provocation methods suchas sleep deprivation, AED tapering, and hyperventilationshould be avoided. Information on electrical safety such asavoiding the equipment coming to contact with water shouldbe provided. All such information is best provided in writingto the patient.

Conclusions and future directions

The ambulatory EEG technology has evolved to become acost-effective alternative for inpatient EEG monitoring. It isa useful test in capturing IED and seizures, which can aiddiagnosis and classification of epilepsy, as well as monitor-ing response to AED therapy, AED withdrawal and predictingprognosis. However, the role of ambulatory EEG in theevaluation of seizures and nonepileptic events, as well aspre-surgical workup in comparison to inpatient VEM is yet tobe established. It is also a useful tool to study sleep-relatedIED and circadian variations in different epilepsy syndromes,an area that has received less attention in the literature.Ambulatory EEG could perhaps be considered an underuti-lized tool as reflected by the fewer number of publicationsin the literature. More well-designed, prospective studiesare needed to define its clinical applications and establishits place as a clinical tool.

Conflict of interest

We confirm that we have read the Journal’s position on issuesinvolved in ethical publication and affirm that this report isconsistent with those guidelines.

Dr. Seneviratne and A/Professor Mohamed report no dis-closures.

Professor Cook has received speaker honoraria from UCBPharma and Sanofi Australia and travel honoraria from UCBPharma and SciGen. He has received research grants from

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

National Health and Medical Research Council (Australia),and Australian Research Council. He has also received aScience, Technology, and Innovation Grant from the StateGovernment of Victoria, Australia.

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A/Professor D’Souza has received travel, investigator-nitiated, and speaker honoraria from UCB Pharma,ducational grants from Novartis Pharmaceuticals and Pfizerharmaceuticals, educational, travel and fellowship grantsrom GSK Neurology Australia, and honoraria from SciGenharmaceuticals.

unding sources

one.

eferences

merican Clinical Neurophysiology Society, 2008. Guideline twelve:guidelines for long-term monitoring for epilepsy. Am. J. Elec-troneurodiagnostic. Technol. 48, 265—286.

minoff, M.J., Goodin, D.S., Berg, B.O., Compton, M.N., 1988.Ambulatory EEG recordings in epileptic and nonepileptic chil-dren. Neurology 38, 558—562.

erg, A.T., Shinnar, S., 1994. Relapse following discontinua-tion of antiepileptic drugs: a meta-analysis. Neurology 44,601—608.

lum, D.E., Eskola, J., Bortz, J.J., Fisher, R.S., 1996. Patient aware-ness of seizures. Neurology 47, 260—264.

ridgers, S.L., Ebersole, J.S., 1985. Ambulatory cassette EEG inclinical practice. Neurology 35, 1767—1768.

ascino, G.D., 2002. Video-EEG monitoring in adults. Epilepsia 43(Suppl. 3), 80—93.

asson, A., Yates, D., Smith, S., Duncan, J., Rodriguez-Villegas, E.,2010. Wearable electroencephalography. What is it, why is itneeded, and what does it entail? IEEE Eng. Med. Biol. Mag. 29,44—56.

hang, B.S., Ives, J.R., Schomer, D.L., Drislane, F.W., 2002. Outpa-tient EEG monitoring in the presurgical evaluation of patientswith refractory temporal lobe epilepsy. J. Clin. Neurophysiol.19, 152—156.

olon, A.J., Ossenblok, P., Nieuwenhuis, L., Stam, K.J., Boon, P.,2009. Use of routine MEG in the primary diagnostic process ofepilepsy. J. Clin. Neurophysiol. 26, 326—332.

ull, R.E., 1985. An assessment of 24-hour ambulatory EEG/ECGmonitoring in a neurology clinic. J. Neurol. Neurosurg. Psychia-try 48, 107—110.

ash, D., Hernandez-Ronquillo, L., Moien-Afshari, F., Tellez-Zenteno, J.F., 2012. Ambulatory EEG: a cost-effective alterna-tive to inpatient video-EEG in adult patients. Epileptic. Disord.14, 290—297.

bersole, J.S., 1985. Ambulatory cassette EEG. J. Clin. Neuro-physiol. 2, 397—418.

bersole, J.S., Bridgers, S.L., 1985. Direct comparison of 3- and8-channel ambulatory cassette EEG with intensive inpatientmonitoring. Neurology 35, 846—854.

bersole, J.S., Leroy, R.F., 1983. Evaluation of ambulatory cassetteEEG monitoring: III. Diagnostic accuracy compared to intensiveinpatient EEG monitoring. Neurology 33, 853—860.

bersole, J.S., Schomer, D.L., Ives, J.R., 2003. Ambulatory EEGmonitoring. In: Ebersole, J.S., Pedley, T.A. (Eds.), CurrentPractice of Clinical Electroencephalography. , 3 ed. LippincottWilliams & wilkins, Philadelphia, pp. 610—638.

aulkner, H.J., Arima, H., Mohamed, A., 2012a. Latency to firstinterictal epileptiform discharge in epilepsy with outpatientambulatory EEG. Clin. Neurophysiol. 123, 1732—1735.

aulkner, H.J., Arima, H., Mohamed, A., 2012b. The utility of pro-

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

longed outpatient ambulatory EEG. Seizure 21, 491—495.ittipaldi, F., Curra, A., Fusco, L., Ruggieri, S., Manfredi, M., 2001.

EEG discharges on awakening: a marker of idiopathic generalizedepilepsy. Neurology 56, 123—126.

IN+ModelE

1

F

F

G

G

G

H

H

I

K

L

L

L

M

M

M

M

M

M

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O

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R

R

S

S

S

S

S

S

S

S

S

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V

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ARTICLEPIRES-4887; No. of Pages 12

2

oley, C.M., Legido, A., Miles, D.K., Chandler, D.A., Grover,W.D., 2000. Long-term computer-assisted outpatient electroen-cephalogram monitoring in children and adolescents. J. ChildNeurol. 15, 49—55.

onseca, C., Silva Cunha, J.P., Martins, R.E., Ferreira, V.M., Marquesde Sa, J.P., Barbosa, M.A., Martins da Silva, A., 2007. A novel dryactive electrode for EEG recording. IEEE Trans. Biomed. Eng. 54,162—165.

illiam, F., Kuzniecky, R., Faught, E., 1999. Ambulatory EEG moni-toring. J. Clin. Neurophysiol. 16, 111—115.

oodin, D.S., Aminoff, M.J., 1984. Does the interictal EEG have arole in the diagnosis of epilepsy? Lancet 1, 837—839.

otman, J., 1982. Automatic recognition of epileptic seizures in theEEG. Electroencephalogr. Clin. Neurophysiol. 54, 530—540.

eers, M., Rampp, S., Kaltenhauser, M., Pauli, E., Rauch, C., Dolken,M.T., Stefan, H., 2010. Detection of epileptic spikes by mag-netoencephalography and electroencephalography after sleepdeprivation. Seizure 19, 397—403.

olter, N.J., 1961. New method for heart studies. Science 134,1214—1220.

ves, J.R., 1975. 4-Channel 24 hour cassette recorder for long-termEEG monitoring of ambulatory patients. Electroencephalogr.Clin. Neurophysiol. 39, 88—92.

oepp, M.J., Farrell, F., Collins, J., Smith, S., 2008. The progno-stic value of long-term ambulatory electroencephalography inantiepileptic drug reduction in adults with learning disability andepilepsy in long-term remission. Epilepsy Behav. 13, 474—477.

ai, C.W., Ziegler, D.K., 1981. Syncope problem solved by continu-ous ambulatory simultaneous EEG/ECG recording. Neurology 31,1152—1154.

each, J.P., Stephen, L.J., Salveta, C., Brodie, M.J., 2006. Whichelectroencephalography (EEG) for epilepsy? The relative useful-ness of different EEG protocols in patients with possible epilepsy.J. Neurol. Neurosurg. Psychiatry 77, 1040—1042.

iporace, J., Tatum, W., Morris, G.L., French, J., 1998. Clinicalutility of sleep-deprived versus computer-assisted ambulatory16-channel EEG in epilepsy patients: a multi-center study.Epilepsy Res 32, 357—362.

arks, D.A., Katz, A., Scheyer, R., Spencer, S.S., 1991. Clinicaland electrographic effects of acute anticonvulsant withdrawalin epileptic patients. Neurology 41, 508—512.

arsan, C.A., Zivin, L.S., 1970. Factors related to the occurrence oftypical paroxysmal abnormalities in the EEG records of epilepticpatients. Epilepsia 11, 361—381.

arson, G.B., McKinnon, J.B., 1972. Miniature tape-recorder formany applications. Control Instrum. 4, 46—47.

artz, G.U., Hucek, C., Quigg, M., 2009. Sixty day continuous use ofsubdermal wire electrodes for EEG monitoring during treatmentof status epilepticus. Neurocrit. Care 11, 223—227.

edical Research Council Antiepileptic Drug Withdrawal StudyGroup, 1991. Randomised study of antiepileptic drug withdrawalin patients in remission. Lancet 337, 1175—1180.

orris 3rd, G.L., Galezowska, J., Leroy, R., North, R., 1994. Theresults of computer-assisted ambulatory 16-channel EEG. Elec-troencephalogr. Clin. Neurophysiol. 91, 229—231.

lson, D.M., 2001. Success of ambulatory EEG in children. J. Clin.

Please cite this article in press as: Seneviratne, U., et al., Theclinical practice: A critical review. Epilepsy Res. (2013), http:/

Neurophysiol. 18, 158—161.xley, J., Roberts, M., 1985. Clinical evaluation of 4-channel ambu-

latory EEG monitoring in the management of patients withepilepsy. J. Neurol. Neurosurg. Psychiatry 48, 930—932.

W

PRESSU. Seneviratne et al.

uy, R.J., 1978. A miniature preamplifier for ambulatory monitor-ing of the electroencephalogram (proceedings). J. Physiol. 284,23P—24P.

iley, T.L., Porter, R.J., White, B.G., Penry, J.K., 1981. The hospitalexperience and seizure control. Neurology 31, 912—915.

ugg-Gunn, F.J., Harrison, N.A., Duncan, J.S., 2001. Evaluation ofthe accuracy of seizure descriptions by the relatives of patientswith epilepsy. Epilepsy Res. 43, 193—199.

alinsky, M., Kanter, R., Dasheiff, R.M., 1987. Effectiveness of mul-tiple EEGs in supporting the diagnosis of epilepsy: an operationalcurve. Epilepsia 28, 331—334.

aravanan, K., Acomb, B., Beirne, M., Appleton, R., 2001. An auditof ambulatory cassette EEG monitoring in children. Seizure 10,579—582.

chomer, D.L., Ives, J.R., Schachter, S.C., 1999. The role of ambu-latory EEG in the evaluation of patients for epilepsy surgery. J.Clin. Neurophysiol. 16, 116—129.

eneviratne, U., Reutens, D., D’Souza, W., 2010. Stereotypy ofpsychogenic nonepileptic seizures: insights from video-EEG mon-itoring. Epilepsia 51, 1159—1168.

eneviratne, U., Cook, M., D’Souza, W., 2012. The electroen-cephalogram of idiopathic generalized epilepsy. Epilepsia 53,234—248.

tefan, H., Hopfengartner, R., 2009. Epilepsy monitoring for ther-apy: challenges and perspectives. Clin. Neurophysiol. 120,653—658.

tefan, H., Kreiselmeyer, G., Kasper, B., Graf, W., Pauli, E.,Kurzbuch, K., Hopfengartner, R., 2011. Objective quantificationof seizure frequency and treatment success via long-term out-patient video-EEG monitoring: a feasibility study. Seizure 20,97—100.

tefan, H., Kreiselmeyer, G., Kerling, F., Kurzbuch, K., Rauch, C.,Heers, M., Kasper, B.S., Hammen, T., Rzonsa, M., Pauli, E.,Ellrich, J., Graf, W., Hopfengartner, R., 2012. Transcutaneousvagus nerve stimulation (t-VNS) in pharmacoresistant epilepsies:a proof of concept trial. Epilepsia 53, e115—e118.

undaram, M., Hogan, T., Hiscock, M., Pillay, N., 1990. Factorsaffecting interictal spike discharges in adults with epilepsy. Elec-troencephalogr. Clin. Neurophysiol. 75, 358—360.

atum 4th, W.O., Winters, L., Gieron, M., Passaro, E.A., Benbadis,S., Ferreira, J., Liporace, J., 2001. Outpatient seizure identifica-tion: results of 502 patients using computer-assisted ambulatoryEEG. J. Clin. Neurophysiol. 18, 14—19.

elis, D., Plouin, P., Gotman, J., da Silva, F.L., 2007. Recommenda-tions regarding the requirements and applications for long-termrecordings in epilepsy. Epilepsia 48, 379—384.

inton, A., Carino, J., Vogrin, S., Macgregor, L., Kilpatrick, C.,Matkovic, Z., O’Brien, T.J., 2004. ‘‘Convulsive’’ nonepilepticseizures have a characteristic pattern of rhythmic artifact distin-guishing them from convulsive epileptic seizures. Epilepsia 45,1344—1350.

ang, L., Liu, Y.H., Wei, L., Deng, Y.C., 2011. The characteristicsand related influencing factors of ambulatory EEGs in patientsseizure-free for 3—5 years. Epilepsy Res. 98, 116—122.

illiamson, P.D., 1992. Frontal lobe seizures. Problems of diagnosisand classification. Adv. Neurol. 57, 289—309.

utility of ambulatory electroencephalography in routine/dx.doi.org/10.1016/j.eplepsyres.2013.02.004

irrell, E., Kozlik, S., Tellez, J., Wiebe, S., Hamiwka, L.,2008. Ambulatory electroencephalography (EEG) in chil-dren: diagnostic yield and tolerability. J. Child Neurol. 23,655—662.