Seizure (2005) 14, 207—212

www.elsevier.com/locate/yseiz

Educational problems with underlying

neuropsychological impairment are common
in children with Benign Epilepsy of Childhood
with Centrotemporal Spikes (BECTS)
K.P. Vinayan a,1, V. Biji b, Sanjeev V. Thomas a,*

a
Department of Neurology, Sree Chitra Tirunal Institute for Medical Sciences and Technology,
Trivandrum, Kerala 695011, India
b
Department of Clinical Psychology, Institute for Communicative and Cognitive
Neurosciences, Trivandrum, India

KEYWORDS Summary
Benign childhood
epilepsy; Introduction: Benign Epilepsy of Childhood with Centrotemporal Spikes (BECTS) is
Centrotemporal spike; one of the most common childhood epilepsies with a good prognosis regarding the
Educational problem; seizure and neuropsychological outcomes. However, recent reports indicate the
Neuropsychological presence of neuropsychological problems in a significant percentage of children with
impairment BECTS. Our study was aimed to examine the educational performance and neurop-
sychological functions along with clinical and electrographic characteristics in a
cohort of children with BECTS.
Methods: We identified a cohort of children with BECTS by screening medical and
EEG recordings of patients attending our institute. Data were collected with a
standard protocol. Their educational performance was evaluated by an interview
with the parents. Neuropsychological and language tests were administered to
children who had educational problems. Statistical analysis was done using the x2-
test.
Results: Fifty children (29 boys and 21 girls; mean age of onset of epilepsy
7.84  2.87 years) who met the criteria for BECTS were included in this study.
Atypical seizure characteristics for BECTS were observed in 26 (52%) children. EEG
showed typical centrotemporal spike and wave discharges in all children, 42% of
them had a tangential dipole in the frontocentral region. An additional extra-
rolandic focus in the EEG was found in seven children (14%). Educational problems
were identified in 27 children (54%); 19 of them had neuropsychological or language
impairment (p = 0.003). We found a statistically significant correlation between the
occurrence of educational problems and the absence of a tangential dipole in the

* Corresponding author. Tel.: +91 471 2524468; fax: +91 471 2446433.
E-mail address: sanjeev@sctimst.ker.nic.in (S.V. Thomas).
1
Present address: Department of Neurology, Amrita Institute of Medical Sciences, Cochin, Kerala 682026, India.

1059-1311/$ — see front matter # 2005 BEA Trading Ltd. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.seizure.2005.01.009
208 K.P. Vinayan et al.

EEG (p < 0.001). Abnormal language function had a significant correlation with
atypical seizure semiology (p = 0.021).
Conclusion: This study shows that a significant number of children with BECTS have
neuropsychological impairment and educational problems.
# 2005 BEA Trading Ltd. Published by Elsevier Ltd. All rights reserved.

Introduction identified neuropsychological impairment and devel-

Epilepsy in children shows considerable polymorph-
ism. Conditions like Lennox—Gastaut Syndrome are
associated with multiple seizures, progressive mental
decline and significant disability. On the other hand,
syndromes like Benign Epilepsy of Childhood with
Centrotemporal Spikes (BECTS) or childhood absence
seizures tend to have a favorable prognosis. BECTS is
one of the most common form of childhood epilepsies
but the reported prevalence varies from 10 to 24%.1,2
It is characterized by the occurrence of partial sei-
zures after 2 years of age associated with normal
neurological and intellectual functions. Typically,
the brief partial, mainly motor seizures are stereo-
typed in semiology, with a nocturnal preponderance.
Family history is often positive.3 The principal elec-
troencephalographic (EEG) criteria include normal
background activity, high amplitude biphasic spikes
followed by prominent slow waves in the mid-tem-
poral (T3, T4) and central (C3, C4) areas, activation of
epileptiform activity during sleep but not during
hyperventilation and occasional generalized spike-
wave discharges.4 Seizures tend to remit sponta-
neously by adolescence. BECTS is generally consid-
ered to be a benign disorder, but several atypical
forms have recently been described.5 Paradoxical
aggravation of seizures, while on antiepileptic drug
(AED) therapy, has also been reported.6 Neuropsycho-
logical functions and psychosocial adjustment of
these children have been studied for over three dec-
ades. One of the earlier studies7 observed mild beha-
vioral or scholastic problems in these children, but
attributed them to parental anxiety and social restric-
tions while another case—control study failed to
demonstrate any difference in intelligence, behavior
or school adjustment.8 Several recent studies have
opmental learning disabilities in these children, but
the clinical relevance of these observations is uncer-
tain. Staden et al.9 demonstrated that children with
BECTS could have selective language dysfunction
(reading, spelling, and auditory verbal learning) even
when their IQ is normal which would suggest a peri-
sylvian dysfunction. Several subtle motor coordina-
tion and neuropsychological impairments have been
identified in a small case—control study.10 Our objec-
tive in this study was to characterize the educational
outcome and neuropsychological profile in a cohort of
children with well-defined clinical and electrographic
features of BECTS.
Methods
Children with clinical and electroencephalographic
features suggestive of BECTS were identified from
medical and EEG records of our institute and were
called for a review at the hospital. Those children
who satisfied the criteria for BECTS (see Table 1)
were included in the study and were evaluated
according to a standard protocol. The ictal semiol-
ogy was described in detail and was classified into
typical and atypical features as described by Loi-
seau.11 Detailed history on treatment, seizure out-
come, peri-natal events, development and family
were obtained. Neurological examination was car-
ried out with special emphasis on soft neurological
signs as described by Touwen.12 EEG details included
background activity and spike characteristics. We
followed Gregory and Wong’s description of frontal
positivity and centrotemporal negativity as the tan-
gential dipole.13 The presence of any associated
extra-rolandic foci was noted separately.

Table 1 Clinical and electrographic criteria for inclusion as BECTS.

Clinical criteria3
1. No neurological or intellectual deficits
2. Onset of seizures after the age of 2 years
3. Brief partial, mainly motor seizures that
are stereotyped in semiology
4. Frequent nocturnal occurrence
5. Family history of epilepsy, especially for
benign types
Electrographic criteria4
1. Normal background activity
2. High amplitude biphasic spikes followed
by prominent slow waves in mid temporal
(T3, T4) and central (C3, C4) areas
3. Activation of epileptiform activity during
sleep but not during hyperventilation
4. Occasional generalized spike-wave discharges
Educational problems with underlying neuropsychological impairment
Educational performance of the child was
assessed in a standard parental interview. The edu-
cational performance was classified as poor if there
were failures in the examinations or if the child was
repeatedly getting low grades in the examinations.
Detailed assessment of neuropsychological and lan-
guage functions were carried out in these children.
Neuropsychological tests included Malins Intelli-
gence Scale for Children (standardized Indian adap-
tation of Wechsler Intelligence Scale),14 Bender—
Gestalt Test,15 Benton Visual Retention Test,16
Seguin Form Board Test17 and Vineland Social Matur-
ity Scale (Indian adaptation).18 The language assess-
ment was done using a structured format with non-
standardized tests available in the vernacular lan-
guage (Malayalam). These included Receptive and
Expressive Emergent Language Scale, Malayalam
Language Test, Malayalam Articulation Test and
Reading Readiness Test in Malayalam. Based on
these tests children were classified into those with
developmental learning disability and those without
developmental learning disability.
Data were analyzed for possible associations
between clinical and EEG features and the educa-
tional performance using the x2-test.
Results
Fifty children (29 boys and 21 girls) who met the
inclusion and exclusion criteria were studied. The
age of onset of seizures ranged from 4 to 13 years
(mean 7.84  2.87 years). Twelve children (24%) had
typical febrile seizures before the onset of epilepsy.
Adverse peri-natal events like pre-maturity, mini-
mal birth asphyxia or neonatal jaundice were
reported in 10 children (20%). There was a history
suggestive of developmental language delay (DLD)
in 15 children (30%). Family history for epilepsy was
present in 13 children (26%). Neurological examina-
tion showed soft neurological signs in 12 children
(24%). Soft neurological signs included adiadocho-
kinesia (10), astereognosis, agraphesthesia and
abnormal deep tendon reflexes (6 each), strabismus
(5), dysarthria and oromotor apraxia (4 each), motor
coordination defects (2), sialorrhea and tremor (1
each). Neuroimaging (CT scan or MRI) was carried
out in 20 children (40%) and was normal in all cases.
Seizure characteristics
More than half of the children (54%) had a combina-
tion of diurnal partial seizures and nocturnal general-
ized seizures. Isolated partial seizures exclusively
during daytime occurred in five children (10%).
Others (36%) had nocturnal generalized seizures only.
209
The typical seizure semiology, characterized by
bucco-facial paresthesias followed by speech arrest,
salivation, brachio-facial or hemi-facial seizures and
occasional nocturnal generalized seizures, was
observed in 48% of children. Atypical ictal semiology
was noticed in 26 children (52%), which included leg
jerking (21), lateral body torsion (5), unilateral body
sensations (5), epigastric pain (2), and ictal blindness
(1). None of the children had status epilepticus or
post-ictal paresis.
EEG characteristics
All patients had at least one EEG typical of BECTS.
Centrotemporal spikes were confined to the left side
for 22 children (44%) and to the right side for 8 (16%)
while others (40%) had bilateral discharges. Gener-
alized spike and wave discharges in addition to
centrotemporal spikes were seen in 20 children
(40%). There were seven children (14%) who had
an extra-rolandic spike focus (parietal, 6; occipital,
1) in addition to the typical centrotemporal focus.
Generalized epileptiform abnormalities were acti-
vated by sleep in 16 children (32%).
The centrotemporal spike discharges showed a
tangential dipole across the fronto-central region
with simultaneous frontal positivity and central or
temporal negativity in 21 children (42%). Among
those who had tangential dipole for the spikes, nine
(42.8%) had atypical seizure semiology and four
(19.0%) had educational problems, whereas among
those who did not express tangential dipole for the
spikes, a larger proportion had atypical seizures (17,
58.6%) or educational problems (23, 79.3%). The
difference was statistically significant ( p < 0.001)
only for the educational problems (see Table 2).
Three children had typical somatosensory evoked
spikes produced by tapping the fingers, as reported
previously.19 Electrical status epilepticus in slow
wave sleep was not seen in any of the children.
Treatment and seizure outcome
In this cohort, 18 children (36%) were treated with
carbamazepine, 11 (22%) with sodium valporate and
11 (22%) with phenobarbitone. The remaining chil-
dren received one of the other AEDs. A change of AED
was rarely instituted. Seizures were controlled in all
children with monotherapy. At the time of evalua-
tion, 13 children (26%) were completely seizure free
for more than 1 year and were off AEDs. Another 13
were seizure free for more than 1 year, but continued
to be on AEDs. 24 children (48%) had seizures in the
previous 1 year and were continuing treatment with
AEDs. Children in the third group had an earlier age of
onset of seizures (mean age 6.83  2.55) compared
210 K.P. Vinayan et al.

Table 2 Clinical and electrographic features of children with and without educational problems.
BECT with educational BECT without educational p
problems problems
N 27 23
Seizure semiology
Typical 11 13 0.017
Atypical 16 10
Neuropsychological abnormalities 19 0 0.003
EEG spike laterality
Left 12 10 0.655
Right 5 3
Bilateral 10 10
Atypical EEG changes 5 2 0.318
Tangential dipole 4 17 <0.001
AED usage
Sodium valproate 8 3 0.261
Carbamazepine 10 8
Phenobarbitone 3 8
Seizure free for >1 year 11 15 0.084

to those in the first two groups (mean age
8.77  2.89, p = 0.01). No statistically significant
differences were observed between these groups
on any of the other clinical, electrographic or neu-
ropsychological variables.
Educational problems and
neuropsychological impairment
Educational problems were identified in 27 children
(54%). Full IQ test was normal in twenty of them and
was borderline in the remaining three children (four
children did not undergo the detailed tests). Detailed
neuropsychological and language tests had confirmed
the presence of minor neuropsychological impair-
ment suggestive of developmental learning disability
in 19 of them. Expressive language impairment and
attention disorder were noticed in nine children
each. There was a statistically significant association
between educational problems and neuropsycholo-
gical impairment including learning disability
( p = 0.003). There was a significant correlation
between occurrence of educational problems and
the absence of the fronto-central dipole for the
spikes in the EEG ( p < 0.001) (see Table 2). Abnormal
language functions had a statistically significant cor-
relation with atypical seizure semiology ( p = 0.021).
Discussion
It is often difficult to estimate the magnitude of
educational problems in childhood epilepsy for want
of precise definitions and criteria.20 Several terms
such as neuropsychological impairment, cognitive
impairment, learning problems, and educational
problems have been used in different studies with
overlapping meanings.
The classical definition of BECTS requires that
there be no neurological or neuropsychological def-
icits. Prediction of the outcome in individual cases
becomes difficult because of the presence of atypi-
cal features and minor neuropsychological impair-
ments.7,9,10 Some of the recent prospective studies
have identified atypical evolutions, clinical fluctua-
tions and significant neuropsychological disabilities
in BECTS.5,21—23 The clinical relevance of these
impairments had remained uncertain. Furthermore,
these cognitive impairments were seldom corre-
lated with any specific EEG or clinical characteris-
tics. There are no population-based studies that
estimate the burden of educational problems in this
seemingly benign epileptic syndrome.
The salient observation in this study was that
more than half (54%) of the children with BECTS
had educational problems. Most of them had under-
lying minor neuropsychological and language
impairments accounting for the educational pro-
blems. It is possible that this cohort of children
drawn from a tertiary center, constitute a subgroup
of BECTS with more associated features, although
the demographic, clinical and electrographic char-
acteristics of this cohort were comparable to those
described earlier.4,24,25
The subgroup of children with educational pro-
blems and neuropsychological impairment had a
Educational problems with underlying neuropsychological impairment
different clinical and electrographic profile when
compared to others. A statistically significant pro-
portion of them had atypical seizure semiology and
had spike discharges without tangential dipole in
their inter-ictal EEG. Earlier studies had shown that
BECTS with tangential dipole for the inter-ictal
epileptiform discharges (IEDs) carries a better prog-
nosis13 with fewer seizures.26 Several inter-ictal EEG
patterns associated with atypical evolutions in
BECTS have been described recently.27 There are
conflicting reports regarding laterality of spikes to
dominant or non-dominant hemisphere and occur-
rence of specific neuropsychological impairments.
Left sided discharges were earlier shown to be
associated with impairment in verbal tasks and
right-sided discharges were associated with non-
verbal tasks.28 In this study, as well as an earlier
study,22 such an association was not confirmed. We
did not observe any significant association between
the educational problems and the laterality of the
IED, presence of extra-rolandic focus or generalized
discharges.
Educational problems in childhood epilepsy can
be divided into state dependent or permanent pro-
blems,29 and the two may co-exist also. Permanent
educational problems are more likely to occur in
Lennox—Gastaut Syndrome and other catastrophic
pediatric epileptic syndromes associated with brain
damage.30 State dependent educational problems
are observed in benign epileptic syndromes and are
potentially reversible. Cognitive adverse effects of
seizures or antiepileptic drugs may contribute to
this.31 Other factors that are associated with edu-
cational problems include mood disorders, poor
self-perception and reduced learning opportu-
nities.20
There are several speculations about the patho-
genesis of neuropsychological impairment in BECTS.
Active IED can interfere with the learning process
and thereby lead to scholastic problems.32 A recent
prospective study has shown that neuropsychologi-
cal functions improved when IEDs were controlled in
children with BECTS.33 Neuropsychological impair-
ments may possibly contribute to the state depen-
dant educational problems in children. Further
studies are necessary in this regard.
Similarities between the syndromes of BECTS,
Landau—Kleffner Syndrome and epilepsy with Con-
tinuous Spike and Wave activities during slow wave
sleep (CSWS) were also highlighted previously.34
Some authors consider them to be part of a broad
continuum of brain maturation disorders with a
marked phenotypic variability, while others con-
sider them to be fundamentally distinct entities.
Genetic studies may possibly help to differentiate
them in future.
211
It appears that BECTS represents a well-defined
pediatric epileptic syndrome with an excellent sei-
zure outcome. A subgroup of children with atypical
seizure semiology and centrotemporal spikes with-
out tangential dipole are likely to have develop-
mental learning disability, minor neuropsychological
impairment and accompanying educational pro-
blems. These children may need special evaluation
and management by a multidisciplinary team.
Acknowledgements
We would like to thank Ms. Vidya and Ms. Anita,
speech pathologists, Institute for Communicative
and Cognitive Neurosciences, Trivandrum, India
for their invaluable contributions in the assessment
of language functions. We also thank Dr. P. Sankara
Sarma and Ms. Sumitra for their help in statistical
analysis.
References
1. Loiseau P, Duche B, Loiseau J. Classification of epilepsies and
epileptic syndromes in two different samples of patients.
Epilepsia 1991;32:303—9.
2. Cavazzuti GB. Epidemiology of different types of epilepsy in
school age children of Modena, Italy. Epilepsia 1980;21:57—62.
3. Holmes GL. Benign focal epilepsies of childhood. Epilepsia
1993;34(Suppl. 3):S49—61.
4. Watanabe K. Benign partial epilepsies. In: Wallace S, editor.
Epilepsy in children. London: Chapman & Hall; 1996. p. 293—
313.
5. Fejerman N, Caraballo R, Tenembaum S. Atypical evolutions
of benign localization-related epilepsies in children: are they
predictable? Epilepsia 2000;41:380—90.
6. Corda D, Gellise P, Genton P, Dravet C, Baldy-Moulinier M.
Incidence of drug induced aggravation in BECTS. Epilepsia
2001;42:754—9.
7. Lerman P, Kivity S. Benign focal epilepsy of childhood: a
follow up study of 100 recovered patients. Arch Neurol
1975;32:261—4.
8. Heijbel J, Blom S, Rasmuson M. Benign epilepsy of childhood
with centrotemporal EEG foci: intelligence, behavior and
school adjustment. Epilepsia 1975;16:679—87.
9. Staden U, Isaacs E, Boyd SG, Brandl U, Neville BG. Language
dysfunction in children with rolandic epilepsy. Neuropedia-
trics 1998;29:242—8.
10. Gunduz E, Demirbelek V, Korkmaz B. Benign rolandic epi-
lepsy: neuropsychological findings. Seizure 1999;8:246—9.
11. Loiseau P. Idiopathic and benign epilepsies. In: Wyllie E,
editor. The treatment of epilepsy–—Principles and practice.
3rd ed. Philadelphia: Lippincott Williams and Wilkins; 2001.
p. 475—84.
12. Touwen BC. Examination of the child with minor neurologi-
cal dysfunction. 2nd ed. Clinics in developmental medicine
no 71. London: William Heinemann Medical Books; 1979.
13. Gregory DL, Wong PK. Clinical relevance of dipole field in
rolandic spikes. Epilepsia 1992;33:36—44.
212
14. Malin AJ. Intelligence scale for Indian children (adaptation
of Wechsler Intelligence Scale for Children). Lucknow:
Indian Psychological Corporation; 1959.
15. Bender L. A visual motor gestalt test and its clinical use.
Research monograph no. 3. New York: American Orthopsy-
chiatry Association; 1938.
16. Benton AL. Benton visual retention test. fifth edition. New
York: The Psychological Corporation; 1991.
17. Cattell RB. Guide to mental testing. 3rd ed. London: London
University Press; 1953.
18. Malin AJ. Vineland social maturity scale (Indian adaptation).
Lucknow: Indian Psychological Corporation; 1970.
19. Rajesh P, Vinayan KP, Thomas SV. Finger tapping elicits spikes
in benign epilepsy with centro-temporal spikes. Neurol India
2002;50:524—5.
20. Lhatoo SD, Sander JWAS. The epidemiology of epilepsy and
learning disability. Epilepsia 2001;42(Suppl. 1):6—9.
21. Wirrell EC, Camfield PR, Gordon KE, Dooley JM, Camfield CS.
Benign rolandic epilepsy: atypical features are very common.
J Child Neurol 1995;10:455—8.
22. Drury I, Beydoun A. Benign partial epilepsy of childhood with
monomorphic sharp waves in centrotemporal and other loca-
tions. Epilepsia 1991;32:662—7.
23. Deonna T, Zesiger P, Davidoff V, Maeder M, Mayor C, Roulet E.
Benign partial epilepsy of childhood: a longitudinal neurop-
sychological and EEG study of cognitive function. Dev Med
Child Neurol 2000;42:595—603.
24. Astradsson A, Olaffson E, Ludvigsson P, Bjorgvinsson H, Hau-
ser WA. Rolandic epilepsy: an incidence study in Iceland.
Epilepsia 1998;39:884—6.
K.P. Vinayan et al.
25. Weglage J, Demsky A, Pietsch M, Kurlemann G. Neuropsycho-
logical, intellectual and behavioral findings in patients with
centrotemporal spikes with and without seizures. Dev Med
Child Neurol 1997;39:646—51.
26. Tsai ML, Hung K. Topographic mapping and clinical analysis of
benign childhood epilepsy with centrotemporal spikes. Brain
Dev 1998;20:27—32.
27. Massa R, de Saint-Martin A, Carcangiu R, Rudolf G, Seegmul-
ler C, Kleitz C, et al. EEG criteria predictive of complicated
evolution in idiopathic Rolandic epilepsy. Neurology 2001;57:
1071—9.
28. Binnie CD, Marston D. Cognitive correlates of inter-ictal
discharges. Epilepsia 1992;33(Suppl. 6):S11—7.
29. Cornaggia CM, Gobbi G. Learning disability in epilepsy:
definitions and classification. Epilepsia 2001;42(Suppl. 1):
2—5.
30. Holmes GL. Pathogenesis of learning disabilities in epilepsy.
Epilepsia 2001;42(Suppl. 1):13—5.
31. Saint-Martin AD, Seegmuller C, Carcangiu R, Kleitz C, Hirsch
E, Marescaux C, et al. Cognitive consequences of Rolandic
epilepsy. Epileptic Disord 2001;3(Spec no. 2):59—65.
32. Deonna T. Rolandic epilepsy: neuropsychology of the active
epilepsy phase. Epileptic Disord 2000;2(Suppl. 1):S59—62.
33. Yung AW, Park YD, Cohen MJ, Garrison TN. Cognitive and
behavioral problems in children with centrotemporal spikes.
Pediatr Neurol 2000;23:391—5.
34. Galanopoulou AS, Bojko A, Lado F, Moshe SL. The spectrum
of neuropsychiatric abnormalities associated with elec-
trical status epilepticus in sleep. Brain Dev 2000;22:
279—95.