ORIGINAL RESEARCH

AQuadruple Examination of Ictal EEG Patterns inMesial TemporalLobe Epilepsy With Hippocampal Sclerosis: Onset, Propagation,

Later Significant Pattern, and Termination

Nermin G. Sirin,* Candan Gurses,* Nerses Bebek,* Ahmet Dirican,† Betul Baykan,* and Aysen Gokyigit*

Purpose: The purpose of this study was to analyze electrophysiologicalproperties of four main stages of ictal patterns of patients with operatedtemporal lobe epilepsy related to hippocampal sclerosis.Methods: We included 48 patients with temporal lobe epilepsy–hippocampalsclerosis. Seizures were classified according to their electrophysiologicalproperties and surgical outcomes as seizure-free and not seizure-free. TheEEGs with artifacts at the beginning were analyzed separately.Results: The most frequent type of ictal onset patterns was rhythmic theta/alphaactivity, which was correlated to seizure-free group, whereas “switch of later-alization” and “bitemporal asynchrony” correlated to not seizure-free group.When bilateral independent ictal propagation patterns emerged, seizures tendedto predict the side of epileptogenic zone wrongly. As a later significant pattern,rhythmic theta/alpha activity lateralized the focus correctly. Seizure terminationwas significantly concordant with hippocampal sclerosis lateralization in theseizure-free group.Conclusion: Ictal onset pattern with rhythmic theta/alpha activity correlateswell with seizure freedom. Morphology of later significant patterns was moreimportant in determining the lateralization reliability than time of appearance.The EEGs with short artifacts at the beginning are seen to be valuable inpresurgical evaluation. Lateralization of ictal termination ipsilateral to MRIindicates good prognosis after surgery. Scalp EEG monitoring helps predictepileptogenic zones and postsurgical outcomes.

Key Words: Temporal lobe epilepsy, Hippocampal sclerosis, Scalp EEG, Ictalpatterns, Ictal propagation patterns, Seizure termination, Postsurgical outcomes.

(J Clin Neurophysiol 2013;30: 329–338)

Hippocampal sclerosis (HS) is usually related with intractableepilepsy (Kim et al., 1999; Semah et al., 1998). Surgical treat-

ment has favorable outcomes when compared with medical therapy(Kumlien et al., 2002; Wiebe et al., 2001; Yasuda et al., 2006).Seizure freedom after appropriate epilepsy surgery is achieved inabout 70% to 90% of patients with HS (Dupont et al., 2006; Engel,2001; Jeong et al., 2005; Jutila et al., 2002; Kilpatrick et al., 1999;Spencer and Huh, 2008; Spencer et al., 2005). In presurgical evalu-ation, the main goal is to identify the localization and lateralization ofthe epileptogenic area by using clinical seizure semiology, interictal

and ictal findings in long-term video-EEG monitoring, neuroimagingdata, and neuropsychological evaluation.

Ictal scalp EEG is considered to be reliable in lateralizing andlocalizing epileptic foci (Ebersole and Pacia, 1996; Pacia and Eber-sole, 1997; Risinger et al., 1989; Serles et al., 2000; Walczak et al.,1992). Especially rhythmic theta and alpha activity are said to bemore accurate and reliable in lateralizing temporal lobe epilepsy(TLE) (Walczak et al., 1992). Ictal scalp EEG propagation patternssuch as “switch of lateralization” and “bitemporal asynchrony” arefound to be associated with poor surgical outcome and bilateralepileptogenicity in several previous studies (Kang et al., 2005; Leeet al., 2006; Schulz et al., 2000; Steinhoff et al., 1995).

The propagation pathways of epileptic discharges and the timeneeded to spread to the contralateral hemisphere have been investigatedin intracranial electrode studies since 1986 (Adam et al., 1994; Liebet al., 1986, 1991; Spencer et al., 1987, 1992), and shorter interhemi-spheric propagation time was found to be related to poor prognosis(Adam et al., 1994; Lieb et al., 1986). Recently, Napolitano and Orriols(2008, 2010) have published two articles that emphasize the valuetemporal and spatial characteristics of scalp ictal EEG propagation indefining intractability and bitemporal excitability.

Although the success of the surgery is favorable in thisdistinctive syndrome, there is a small percentage of patients whocontinue to have seizures after standard surgical procedures. We knowthat ictal scalp EEG is very useful in determining the localization andlateralization of the epileptogenic area and the prognosis after surgery(King et al., 1997; Pataraia et al., 1998; Risinger et al., 1989; Schulzet al., 2000). In this study, our aim was to investigate the prognosticsignificance of ictal scalp EEG patterns and propagation characteristicsin TLE related to HS.

MATERIALS AND METHODS

Patient SelectionWe reviewed patients with TLE, diagnosed according to their

clinical and electrophysiological features, who were followed by theepilepsy outpatient clinic of our department between 1999 and 2010.Patients fulfilling the following criteria were included in the study: (1)cranial MRI evidence of HS (Gurses et al., 2007), (2) medically refrac-tory epilepsy with operation, and (3) pathologically diagnosed with HS.All patients were followed up for at least 1 year after the surgery.According to the Engel classification, the patients were classified asseizure-free (Engel Class I) and not seizure-free (Engel Class II–IV)(Wieser et al., 2001).

All patients underwent extensive presurgical evaluation, includ-ing prolonged video-EEG monitoring with scalp electrodes, recordingat least one seizure. Ictal EEG data were stored digitally and retrievedusing 32 to 64 channels for analysis (Nihon Kohden or Medelec

From the *Departments of Neurology and †Biostatistics, Istanbul Faculty of Medicine,Istanbul University, Capa, Fatih, Istanbul, Turkey.

Supported by Istanbul University Scientific Research Projects (Project Number:3605, 2009–2011).

Poster presented at American Clinical Neurophysiology Society 2012 AnnualMeeting, February 7–12, 2012, San Antonio, Texas.

Address correspondence and reprint requests to Nermin G. Sirin, MD, Departmentof Neurology, Istanbul Faculty of Medicine, Istanbul University, Capa, Fatih,Istanbul 34093, Turkey; e-mail: gorkemsirin@yahoo.com.tr.

Copyright � 2013 by the American Clinical Neurophysiology SocietyISSN: 0736-0258/13/3004-0329

Journal of Clinical Neurophysiology � Volume 30, Number 4, August 2013 329

software). Scalp electrodes were placed according to the international 10to 20 system with the addition of anterior temporal electrodes of T1–T2;some patients had extra Cheek electrodes (Ch1–2). Referential andbipolar montages were used. Seizures were assessed by two experiencedelectroencephalographers independently (C.G., N.B.). One of them wasblinded for all other data of the patients.

Ictal EEG AnalysisIctal discharges were classified according to the following

criteria (Steinhoff et al., 1995):

1. Pattern of ictal discharges:a. Attenuation of background activity (if only lateralized)

(Fig. 1).b. Cessation of interictal epileptiform discharges.c. Repetitive spiking (Fig. 2).d. Rhythmic delta activity.e. Rhythmic theta/alpha activity.f. Rhythmic beta activity.

2. Location of ictal discharges:a. Temporal: the amplitude ratio of temporal versus para-

sagittal chains is higher than 2:1 in bipolar montages.b. Hemispheric: the amplitude ratio of temporal versus para-

sagittal chains is less than 2:1 in bipolar montages.

3. Lateralization of ictal discharges:a. Unilateral right/left: the amplitude ratio between 2 sides

is higher than 2:1 in referential montages.b. Bilateral right/left: the amplitude ratio between 2 sides is

higher than 1:1 but less than 2:1 in referential montages.c. Nonlateralized: the amplitude ratio between 2 sides is 1:1.

First, seizures were divided into 2 groups: (1) seizures withoutartifacts at onset and (2) seizures with artifacts at onset. Ictaldischarges were then evaluated in 5 main stages (I–V) (Fig. 3).Seizures with artifacts were analyzed separately and were notincluded in the group of without artifacts.

In seizures without artifacts at the onset:

I. Morphology of patterns at onset (the first unequivocal EEGchange that lasted for 3 seconds) were classified as followsaccording to the criteria mentioned above (Schulz et al., 2000;Steinhoff et al., 1995).II. Lateralization of the seizures were classified according to thelateralization of pattern at onset and later propagation patterns:

a. Unilateral temporal/hemispheric.b. Bilateral temporal/hemispheric.c. Nonlateralized.d. Lateralized at ictal EEG onset followed by (1) lateralization

switched to the contralateral temporal/hemisphere-“switch

FIG. 1. Attenuation of background activity (arrows) in the right hemisphere as an ictal onset.

N. G. Sirin et al. Journal of Clinical Neurophysiology � Volume 30, Number 4, August 2013

330 Copyright � 2013 by the American Clinical Neurophysiology Society

of lateralization” or (2) bitemporal asynchronous ictal EEGpattern, defined as more than 1 Hz frequency differencebetween 2 sides. In both patterns, the duration of activitymust be.10 seconds (Steinhoff et al., 1995) (Figs. 4A–C).

III. Later significant pattern was determined as a change in the mor-phology of the onset pattern that appeared after 3 seconds followingthe patterns at onset and lasted .10 seconds. The morphologicalpattern, location, and lateralization of these discharges were notedas later significant patterns (Serles et al., 2000; Steinhoff et al., 1995).

For seizures with artifacts, we analyzed the durations ofartifacts an the morphology, location, and lateralization of ictaldischarges seen after the artifacts had disappeared.

After classifying the seizures, patients were grouped accordingto their seizure recordings without artifacts as the following: (Onlypatients with two or more seizures recorded could be evaluated for thispart. Patients with two recorded seizures one of whose seizures wasnon-lateralized were not included.) (Schulz et al., 2000)

1. Patients whose all ictal EEGs were lateralized to one temporalregion/hemisphere (one nonlateralized seizure was allowed).

2. Patients whose all ictal EEGs were nonlateralized (one later-alized EEG was allowed).

3. Patients with a “switch of lateralization” or “bitemporal asyn-chrony” in at least one seizure.

4. Patients with ictal EEGs showing independent seizures fromeach temporal region/hemisphere.

IV. Usual propagation:

Propagation of ictal discharges could be assessed in seizureswithout artifacts and ictal EEGs unilaterally lateralized to onetemporal region/hemisphere. The following variables wererecorded:

Spatial characteristics of propagation (Napolitano and Orriols,2010):

1. Ictal EEG lateralized initially to unilateral temporal electrodesa. None or with propagation only to ipsilateral electrodes.b. With propagation first to ipsilateral electrodes, then par-

tially to contralateral electrodes.c. With propagation simultaneously to ipsilateral electrodes

and all of the contralateral electrodes.d. With propagation to contralateral electrodes (partially or

totally) without involving the other ipsilateral electrodeswhich were spared at the start of the seizure initially.

2. Ictal EEG lateralized to unilateral hemispheric electrodesinitiallya. No propagation to contralateral electrodes.b. With partial propagation to contralateral electrodes.

Ictal EEG termination is defined as complete resolutionof rhythmic activity to slow, disorganized or flat backgroundactivity without any paroxysmal discharges (Spencer andSpencer, 1996). We analyzed all seizures for ictal EEG termi-nation and determined the location and lateralization of offset(Fig. 5).

FIG. 2. Left frontotemporal ictalonset (arrow) by repetitive spiking.

FIG. 3. Diagram of ictal EEG evaluation.

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Copyright � 2013 by the American Clinical Neurophysiology Society 331

Statistical AnalysisThe analysis was performed with SPSS software (Statistical

Package for the Social Science, version 15.0, Chicago, IL).According to the distribution and characteristics of data, propertests such as Fischer exact test, x2 test, Kruskal–Wallis test,

Mann–Whitney U test and independent samples t-test were used.Fischer exact test and x2 test were used to compare the ratios ofindependent groups. Mann–Whitney U test was used to comparethe median values of independent groups when there were twogroups and Kruskal–Wallis test was used when there were more

FIG. 4. A–C, An example of “switch o flateralization”and “bitemporal asynchrony.” Left frontotemporal ictalonset by rhythmic delta activity starts (arrow). After 10seconds, rhythmic theta activity appears in the sameregion (5-pointed star). After 20 seconds, 4-pointed starmarks the switch of lateralization of the ictal dischargesto right frontotemporal electrodes.

N. G. Sirin et al. Journal of Clinical Neurophysiology � Volume 30, Number 4, August 2013

332 Copyright � 2013 by the American Clinical Neurophysiology Society

than two groups. Independent sample t-test was used to comparethe mean values of independent groups. The interobserverreliability was assessed by Cohen kappa and contingency coeffi-cient tests.

RESULTSWe studied 222 seizures from 48 patients retrospectively.

Of these seizures, 32 were not included because they eitherconsisted solely of artifacts or for other problems in data storageretrieval. Patients with invasive recordings were not included inthe groups. Thirty-eight seizures with shorter artifacts at onsetwere analyzed separately. A total of 190 seizures of 48 patientswere included in the study. Clinical features of the patients arelisted in Table 1.

Seizures Without Artifacts at OnsetOne hundred and fifty-two seizures from 42 patients were

examined (on average 3.6 seizures per patient; range, 1–11). Themost frequent pattern at onset was rhythmic theta/alpha activity(82/152; 53.9%). Later significant patterns in 25 seizures could notbe analyzed because of artifacts. Sixty-eight (53.5%) of 127 seizureshad one of the later significant patterns mentioned above. Table 2summarizes the ictal EEG findings.

Table 3 shows that the most frequent pattern in seizure-free group was rhythmic theta/alpha activity (62.3%), whereas innot seizure-free group, rare patterns (attenuation of backgroundactivity, cessation of interictal epileptiform discharges, repetitivespiking) were seen (59.1%). Within seizure-free group, 82.3%of seizures were unilateral and only 12.3% of seizures hadbilateral independent ictal propagation patterns (“switch oflateralization/bitemporal asynchrony”), but within not seizure-free group, these were 54.5% and 40.9%, respectively (P ¼0.004; Table 3, Fig. 6). There was no relation between

lateralization of later significant patterns and surgical outcomes(Table 3).

In seizure-free group, ictal EEG lateralization was correct(concordant with the operated side) in all seizures whose pattern at

FIG. 5. Left hemispheric terminationof ictal discharges (arrow).

TABLE 1. Clinical Features of the Study Group

Gender (M/F) 25/23Mean age (range), year 37.8 6 8 (22–66)Mean age of epilepsy onset (range), year 11.5 6 8.4 (1–34)Risk factors (febrile seizures, encephalitis, etc.), n (%)Present 43 (89.6)Absent 5 (10.4)

Mean follow-up (range), year 6.6 6 3.2 (2–12)MRI findingsdside of HS, n (%)Right 20 (41.7)Left 24 (50)Bilateral 1 (2.1)Bilateral, right . left 3 (6.3)

Mean age at surgery (range), year 30.4 6 8 (15–63)Mean duration of epilepsy until surgery (range), year 19 6 8.2 (6–39)Type of surgery, n (%)Selective amygdalohippocampectomy 22 (45.8)Amygdalohippocampectomy 15 (31.3)Amygdalohippocampectomy and anterior temporallobectomy

9 (18.8)

Selective amygdalohippocampectomy anduncusectomy

2 (4.2)

Side of operation, n (%)Right 23 (47.9)Left 25 (52.1)

Surgical outcome, n (%)Seizure-free 43 (89.6)Not seizure-free 5 (10.4)

HS, hippocampal sclerosis.

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onset was attenuation of background activity, cessation ofinterictal epileptiform discharges or repetitive spiking, and in92.7% and 91.4% of seizures rhythmic delta activity and rhythmictheta/alpha activity, respectively. Seizures with bilateral indepen-dent seizure propagation (16%) were more likely to be lateralizedwrongly than the ones that do not have this property (1%, P ¼0.002). As a later significant pattern, 96.7% of seizures that wererhythmic theta/alpha activity and 66.7% of seizures that wererhythmic delta activity lateralized the focus correctly. Rhythmicdelta activity, as a later significant pattern, lead to wrong lateral-ization more frequently than the others (P ¼ 0.02). All seizureswhose latter significant patterns were repetitive spiking lateralizedthe focus correctly. There was no relation between the time ofappearance of later significant patterns and correct lateralization(Table 4).

Seizures With Artifacts at the BeginningThere were 38 seizures from 11 patients with artifacts at

the beginning. The mean duration of the artifacts was 21.1 615.5 seconds (range, 3–75 seconds, only in 3 of the patients theywere .40 seconds). The ictal discharges were lateralized in 31seizures (81.6%) and nonlateralized in 7 seizures (18.4%). There

was no relation between the surgical outcome and lateralizationof the ictal discharges after the artifacts. “Switch of lateraliza-tion/bitemporal asynchrony” after artifacts was more frequent innot seizure-free group (Table 3).

Usual Propagation PatternsThe usual propagation patterns could be examined in seizures

that were restricted to 1 temporal/hemispheric electrodes. Onehundred and four seizures from 34 patients were analyzed accordingto particular sequences and the most frequent pattern was propaga-tion to the contralateral electrodes sequentially (Table 2). The rela-tion between surgical outcomes and usual propagation patterns isshown in Table 3.

Lateralization of Individual PatientsPatients with less than two recorded seizures and patients

with two recorded seizures one of whose seizures was non-lateralized were not included in the analysis. Hence, 36 patientswere taken into account. The groups of patients according to theirlateralization are shown in Table 2. Patients with “switch of later-alization” and/or “bitemporal asynchrony” were more likely to bein not seizure-free group, whereas patients whose seizures werelateralized were in seizure-free group (Table 3).

Seizure TerminationSeizure termination was analyzed in 124 seizures from 39

patients. Seizure termination was lateralized in 107 seizures (86.3%)and nonlateralized in 17 seizures (13.7%). Seizures that hadtermination ipsilateral to the onset lateralization were more frequentin seizure-free group (88.2%) than in not seizure-free group (53.8%,P ¼ 0.002; Table 3, Fig. 7). Without taking seizure onset into con-sideration, seizure termination was more likely to be ipsilateral to theside of MRI in seizure-free group than in not seizure-free group (P ¼0.004; Table 3).

Interobserver ReliabilityFor the analysis of interobserver reliability, each observer

examined 152 seizures without artifacts at the beginning from 48patients. The patterns at onset, lateralization of patterns at onset,and lateralization of individual patients were determined. Inter-observer reliability in terms of these parameters was good toexcellent (for pattern at onset contingency, coefficient valueis 0.81; for lateralization of patterns at onset, kappa value is0.88; and for classification of patients, contingency coefficientvalue is 0.83).

DISCUSSIONWe investigated all noteworthy aspects in ictal EEG

monitoring, including patterns at onset, later significant patterns,propagation and termination in patients with operated HS. Wealso included ictal EEGs with short-lasting artifacts, which hasso far been neglected despite its practical clinical necessity, inthis study.

Rhythmic theta/alpha activity, which had been related toTLE and/or HS in previous studies, was found to be the mostfrequent pattern at onset, originating mostly from hippocampalregions (Assaf and Ebersole, 1999; Caboclo et al., 2007; Ebersole

TABLE 2. Ictal EEG Findings

Pattern at onset, n (%)Attenuation of background activity 6 (3.9)Cessation of interictal epileptiformdischarges

1 (0.7)

Repetitive spiking 14 (9.2)Rhythmic delta activity 49 (32.2)Rhythmic theta/alpha activity 82 (53.9)

Lateralization of seizures, n (%)Unilateral 119 (78.3)Bilateral/nonlateralized 8 (5.3)Switch of lateralization/bitemporal asynchrony 25 (16.4)

Later significant patterns, n (%)Repetitive spiking 7 (10.3)Rhythmic delta activity 22 (32.4)Rhythmic theta/alpha activity 39 (54.7)

Lateralization of seizuresdlater significantpatterns, n (%)

Unilateral 66 (97.1)Bilateral/nonlateralized 2 (2.9)

Usual propagation patterns, n (%)Group a: none or with propagation only toipsilateral electrodes

24 (23.1)

Group b: with propagation to ipsilateral electrodesand then partially to contralateral electrodes

56 (53.8)

Group c: with propagation simultaneously toipsilateral electrodes and all of thecontralateral electrodes.

21 (20.2)

Group d: with propagation to contralateral electrodespartially or totally without involving theipsilateral electrodes spared initially.

3 (2.9)

Classification of patients, n (%)Patients with only lateralized ictal EEGs 26 (72.2)Patients with only nonlateralized ictal EEGs 1 (2.8)Patients with “switch of lateralization”or “bitemporal asynchrony”

9 (25.8)

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and Pacia, 1996; O’Brien et al., 1996; Pacia and Ebersole, 1997;Pataraia et al., 1998; Steinhoff et al., 1995; ). Concordant withprevious studies, we found that the most frequent pattern at onsetis rhythmic theta/alpha activity also in patients with TLE associ-ated with HS. In addition, rhythmic theta/alpha activity was seento be more frequent in the later seizure-free group, whereas rarepatterns, such as attenuation of background activity, cessation ofinterictal epileptiform discharges, and repetitive spiking, weremore frequent in the not seizure-free group. Likewise, Steinhoffet al. (1995) showed that in seizure-free patients after anteriortemporal lobectomy, rhythmic theta/alpha activity was the mostfrequent pattern at onset.

Although some studies underestimate the value of seizure-onset lateralization and take into consideration only the cranialMRI and interictal EEG findings (Castro et al., 2008; Cukiert et al.,2009; Gilliam et al., 1997), these present important data forthe presurgical evaluation of prognosis (Schulz et al., 2000). We

demonstrated that “switch of lateralization” and “bitemporalasynchrony” are related to worse prognosis after surgery in TLEassociated with HS. Moreover, in the presence of these patterns,seizure-onset lateralization was more likely to be incorrect. Whenthese patterns are ignored, surgical outcomes prove to be poor. Thisfurther indicates the importance of ictal recording. Nevertheless,the small size of the not seizure-free group needs to be noted asa disadvantage. Larger studies are needed to acquire more detailedinformation about ictal EEG findings.

The most frequent later significant pattern was alsorhythmic theta/alpha activity in TLE associated with HS in thepresent study. Rhythmic theta/alpha activity and other rare latersignificant patterns perfectly lateralized the epileptic focuscorrectly, as also indicated by Steinhoff et al. (1995). Rhythmicdelta activity as a later significant pattern was more likely to berelated to wrong lateralization. Since we found no relationbetween the time of appearance of later significant patterns and

TABLE 3. Association of Surgical Outcomes and Ictal EEG

Seizure-Free, n (%) Not Seizure-Free, n (%) P

Patterns at onset 0.000*Rare patterns† 8 (6.2) 13 (59.1)Rhythmic delta activity 41 (31.5) 7 (31.8)Rhythmic theta/alpha activity 81 (62.3) 2 (9.1)

Lateralization of seizure 0.004*Unilateral 107 (82.3) 12 (54.5)Bilateral/nonlateralized 7 (5.4) 1 (4.5)Switch of lateralization/bitemporal asynchrony 16 (12.3) 9 (40.9)

Switch of lateralization/bitemporal asynchrony inseizures with artifacts at the beginning

0.02‡

Present 2 (5.7) 2 (66.7)Absent 33 (94.3) 1 (33.3)

Usual propagation patterns 0.01*Group a 14 (15.9) 10 (62.5)Group b 51 (58) 5 (31.3)Group c 20 (22.7) 1 (6.3)Group d 3 (3.4) 0 (0)

Concordance of lateralization of later significantpatterns and MRI

.0.05*

Ipsilateral 50 (86.2) 9 (90)Contralateral 6 (10.3) 1 (10)Bilateral/nonlateralized 2 (3.4) 0 (0)

Classification of patients 0.04*Patients with only lateralized ictal EEGs 25 (78.1) 1 (25)Patients with only nonlateralized ictal EEGs 1 (3.1) 0 (0)Patients with “switch of lateralization” or“bitemporal asynchrony”

6 (18.8) 6 (75)

Seizure termination§ 0.002*Ipsilateral to the seizure onset 67 (88.2) 7 (53.8)Contralateral to the seizure onset 9 (11.8) 6 (46.2)

Concordance of seizure termination and MRI 0.004*Ipsilateral 84 (77.1) 10 (66.7)Contralateral 8 (7.3) 5 (33.3)Nonlateralized 17 (15.6) 0 (0)

Group a: none or with propagation only to ipsilateral electrodes. Group b: with propagation to ipsilateral electrodes and then partially to contralateral electrodes. Group c: withpropagation simultaneously to ipsilateral electrodes and all of the contralateral electrodes. Group d: with propagation to contralateral electrodes partially or totally without involving theipsilateral electrodes spared initially. Significant P values are written in boldface.

*Pearson x2.†Attenuation of background activity, cessation of interictal epileptiform discharges, and repetitive spiking.‡Fischer exact test.§only seizures with both termination and onset evaluations were included in the analysis.

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the correct lateralization, it can be said that the morphology oflater significant pattern was more important in determining thelateralization reliably than the time of appearance.

Previous intracranial electrode studies with mesial TLEpatients showed that the most frequent propagation was first toipsilateral frontal lobe, then to contralateral frontal lobe, and finallyto contralateral temporal lobe (Adam et al., 1994; Lieb et al.,1991). Recently, Napolitano and Orriols (2010) stated that propa-gation patterns in ictal scalp EEG are almost always gradual andsequential, and they related this finding to unilateral excitabilityand lower degree of intractability. Similarly, our study alsorevealed that the most frequent propagation pattern was sequential.However, we did not find an association between propagation andexcitability and/or intractability, which may be explained in relationto the methodological differences, especially their outcome

parameters. Furthermore, we have worked on patients with patho-logically proven HS, a more specific group in TLE.

When assessing the relation between these patterns andsurgical outcomes, in seizure-free group, the sequential propaga-tion pattern (Group b) was more frequent; and in not seizure-freegroup, seizures without propagation or with propagation only toipsilateral electrodes were more frequent. However, 10 of theseizures in Group a belong to the same patient, which may requireverification of this datum in more cases. Hence, these seizures andthe seizures in Group d, because of uncertainty about thehippocampal commissure, were excluded from the analysis (Liebet al., 1986; Spencer et al., 1987). Of the seizures in seizure-freegroup 23.5% and of the seizures in not seizure-free group 16.7%were in Group c, whereas 76.5% of the seizures of the former and83.3% of the latter were in Groups a and b. The P-value was found

FIG. 6. Association between surgical outcomesand lateralization of seizure.

TABLE 4. Lateralization of EEG Seizure Onset Versus Patterns at Onset, Later Significant Patterns, and Switch of Lateralization/Bitemporal Asynchrony*

Correct Wrong Non-Lat. P

Patterns at onset, n (%) .0.05†Rare patterns‡ 8 (100) 0 (0) 0 (0)Rhythmic delta activity 38 (92.7) 1 (2.4) 2 (4.9)Rhythmic theta/alpha activity 74 (91.4) 4 (4.9) 3 (3.7)

Switch of lateralization/bitemporal asynchrony, n (%) 0.002†Present 21 (84) 4 (16) 0 (0)Absent 95 (95) 1 (1) 4 (4)

Later significant patterns, n (%) 0.02†Repetitive spiking 7 (100) 0 (0) 0 (0)Rhythmic delta activity 14 (66.7) 5 (23.8) 2 (9.5)Rhythmic theta/alpha activity 29 (96.7) 1 (3.3) 0 (0)

Median time of appearance of later significant patterns, s 15.5 9 14.5 0.08§

Non-lat, non-lateralized.*Seizures of patients in seizure-free group were assessed.†Pearson x2.‡Attenuation of background activity, cessation of interictal epileptiform discharges, and repetitive spiking.§Nonparametric testdKruskal–Wallis.

N. G. Sirin et al. Journal of Clinical Neurophysiology � Volume 30, Number 4, August 2013

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insignificant. Although there are studies done with intracranialelectrodes for exact propagation pathways, this is the first studyto show propagation in TLE associated with HS using scalp elec-trodes, which was formerly thought to be unlikely.

In ictal scalp EEGs, we found that seizure terminationipsilateral to the seizure onset was related to good surgicaloutcome in patients with TLE associated with HS. Besides theonset lateralization, seizure termination ipsilateral to MRI was alsorelated to good surgical outcome. The lateralization of seizuretermination provides invaluable information for the determinationof the epileptogenic zone. In literature, seizure termination islimited to intracranial electrode studies and there are no scalp EEGstudies (Spencer and Spencer, 1996; Verma et al., 2001). Theresults of those studies with intracranial electrodes are in agree-ment with this present study. Our study is the first to demonstratethe importance of seizure termination pattern in noninvasive pre-surgical evaluation.

Artifacts are the most important problems in EEG interpre-tation, and they become all the more challenging in ictal EEGs. Inthis study, we aimed to examine the ictal discharges after the onset ofartifacts and tried to determine their significance. Ictal dischargesafter artifacts were seen to be mostly lateralized but have no relationto prognosis. “Switch of lateralization” and “bitemporal asynchrony”were related to worse prognosis even when they were seen afterartifacts. Despite the presence of artifacts, such data revealed afterthe artifact convey significantly useful information regarding prog-nosis and surgical outcomes. In our study, separation of seizures withand without artifacts at onset and relating “later significant pattern”findings to surgical outcome has been particularly useful, as epilep-tologists frequently come across similar situations in clinical prac-tice. We emphasize the importance of taking into considerationseizures both with and without artifacts at onset and their “latersignificant pattern.”

CONCLUSIONOur results demonstrate that the most frequent ictal onset

pattern is rhythmic theta/alpha activity, which we correlated with theseizure-free group, whereas “switch of lateralization” and “bitempo-ral asynchrony” were both correlated to the not seizure-free group.

The morphology of latter significant patterns was observed to bemore important in determining the lateralization reliability than thetime of appearance. The correlation between propagation and surgi-cal outcomes was found to be statistically significant; however,because the results are based on a limited number of patients, theyneed to be verified with larger series. Ictal scalp EEG with shortartifacts at the beginning is seen to be valuable in presurgical eval-uation. Lateralization of ictal termination ipsilateral to MRI indicatesgood prognosis in patients with HS after surgery. Scalp EEG mon-itoring provides useful information for the prediction of epilepto-genic zones and postsurgical outcomes in patients with TLE andpathologically proven HS.

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