ARTICLE
Auteur(s) : Amit Ray1, Prakash Kotagal2
1Department of Neurology, Fortis Hospital, Delhi,
India
2Section of Pediatric Epilepsy, Cleveland Clinic
Foundation, Cleveland, Ohio, USA
Article reçu le 21 Février 2005, accepté le 8 Septembre 2005
Although the semiology of temporal lobe epilepsy (TLE) has been
studied in detail in adults, relatively few studies have examined
TLE in infants and children. The TLE syndrome in adults is a rather
homogeneous entity, with mesial temporal (hippocampal) sclerosis,
its commonest neuropathological substrate. The distinct
neuropathological correlates associated with this entity include
neuronal loss in the hippocampus (the CA1 region being the most
profoundly affected, with relative sparing of the CA2 region). The
imaging correlates of these pathological changes, as demonstrated
by high resolution MRI studies, include 1) an increased signal in
the hippocampus, best appreciated on FLAIR sequences, 2)
hippocampal volume loss, best appreciated on the T1 coronal images,
3) an overall homogeneous appearance of the hippocampus (as opposed
to the gray – white demarcation usually found in normal
hippocampi). Whether the hippocampal neuron loss precedes the
seizure onset or is a result of ongoing seizures, especially
prolonged seizures, is a question which has not yet been
satisfactorily answered. However, there is some evidence to suggest
that this is an ongoing process, which evolves over time, including
following the development of seizures (French et al. 1993, Mathern
et al. 1995). The relationship between a past history of febrile
seizures in early childhood, especially complex febrile seizures,
and the development of the mesial temporal sclerosis (MTS) syndrome
in later life is also a matter of considerable debate and
controversy, with contradictory evidence, both in favor of and
against this association, presented in several studies (Cendes et
al. 1993, French et al. 1993, Hudson et al. 1993, Hufnagel et al.
1994, So et al. 1989, Williamson et al. 1993). As a high proportion
of these patients are medically refractory to currently available
antiepileptic drug therapy, temporal lobectomy offers them a very
good chance for seizure-freedom after resective surgery (Engel et
al. 2003).In contrast to its adult counterpart, childhood-onset TLE
probably represents a distinct nosological and probably less
homogeneous syndrome, with MTS being relatively less common in this
age group. Duchowny et al. (1992) studied 16 children less than 12
years old, with medically refractory seizures of temporal lobe
origin who underwent a standard anterior temporal lobectomy. They
found prenatally-acquired abnormalities of neurogenesis
(malformations of cortical development, migrational disturbances),
low-grade neoplasms, tuberous sclerosis (TS) to be much more
frequent, whereas MTS was found in only two children. Even in those
two cases, MTS was not an isolated finding (coexistent hamartoma in
one and cortical dysplasia in the other).We present a brief review
of seizure semiology in the better-studied, adult onset TLE
syndrome followed by a detailed discussion of the childhood
syndrome highlighting the inherent differences between these two
entities
Semiology of temporal lobe epilepsy in adults
Clinical symptomatology (Kotagal et al. 1995) includes typical
auras (the abdominal aura often commonly described as an
“epigastric rising sensation” is commonest), fear, déjà vu- or
jamais vu-like sensations (King and Ajmone-Marsan 1977, Palmini and
Gloor 1992, Van Buren 1963), olfactory or gustatory hallucinations.
Auras are extremely common in patients with mesial temporal lobe
epilepsy occurring in more than 90% cases and on occasion may be
the only manifestation of the seizure. In most cases however, this
aura is followed by other manifestations which may include motor
and behavioral arrest, the so-called “blank stare” with retraction
of the palpebral fissures accompanied by pupillary dilatation,
decreased responsiveness and alteration of consciousness.
Automatisms are another common feature of mesial temporal lobe
seizures, and are described as semi-purposeful, stereotyped motor
activities. Commonly described automatisms are oro-alimentary
(lip-smacking and swallowing, chewing, licking) and in the distal
upper extremities (picking or fumbling movements).
Contralateral dystonic posturing (most commonly seen in the
hand, but occasionally seen in the face and leg), has been long
recognized as a manifestation of temporal lobe seizures, but was
only relatively recently recognized as an important lateralizing
sign (Kotagal et al. 1989). Figures ranging between 15-70% have
been quoted regarding the frequency of this sign in mesial temporal
epilepsy, however, the lateralizing specificity of this sign is
extremely high (90-100%). Studies utilizing ictal SPECT have
concluded that this unilateral, dystonic posturing is the clinical
correlate of increased perfusion in the basal ganglia ipsilateral
to the side of seizure onset.
A summary of features seen in this subtype of TLE is shown in
table 1( Table 1 ).
Table 1 Features of temporal lobe epilepsy in different
age-groups.
|
Characteristic
|
- Infants and toddlers
- (0-3 years)
|
- Pre-school and early school
- (3-6 years)
|
Older children, adolescents and adults
(> 6 years)
|
|
Etiology
|
Cortical dysplasia, Low grade neoplasms, Tuberous sclerosis, etc;
hippocampal sclerosis uncommon
|
Cortical dysplasia, low grade neoplasm; HS less common
|
Hippocampal sclerosis is commonest; dysplasia, low grade neoplasm,
or vascular malformation
|
|
Semiology
|
|
Auras
|
Rare or difficult to recognize
|
May be present
|
Common, especially abdominal aura
|
|
Motor phenomena
|
Prominent motor manifestations; tonic, clonic, myoclonic which may
be bilateral and symmetric
|
Less prominent motor manifestations; may show dystonic posturing or
version
|
Less motor phenomena; contralateral dystonic posturing is
common.
|
|
Automatisms
|
Common; simple in character; usually oroalimentary
|
Common; more complex with increasing age; hand automatisms in
addition to oroalimentary
|
Common; complex and more discrete; oral, hand and verbal
automatisms
|
|
EEG
|
|
Interictal phenomena
|
Extratemporal and generalized sharp waves, commonly seen in
addition to temporal spikes especially in patients with
tumors(Wyllie et al. 1993, Brockhaus and Elger 1995, Wyllie E
1995)
|
Anterior temporal sharp waves; extratemporal or contralateral
temporal sharp waves are often seen (Mohamed et al., 2001)
|
Unilateral sharp waves maximum at the sphenoidal or anterior
temporal electrodes
|
|
Ictal EEG
|
Poorly localized/falsely lateralized (occasionally generalized)
seizure patterns especially in patients with tumors (Wyllie et al.
1993, Brockhaus and Elger 1995, Wyllie E 1995)
|
Usually lateralized and maximum in the temporal electrodes
|
Usually well localized seizure patterns from ipsilateral temporal
lobes with maxima at sphenoidal or anterior/inferior temporal
electrodes
|
|
Imaging
|
Tumor, dysplasia
|
Tumor, dysplasia, less common HS
|
Increased FLAIR signal, with hippocampal atrophy
|
|
Pathology
|
Dysplasia, low grade tumor etc
|
Low grade tumor, dysplasia, hippocampal sclerosis
|
Hippocampal sclerosis
|
TLE in children
Epilepsies (both focal and generalized at onset) in infants and
young children have a limited repertoire of ictal manifestations.
Duchowny (1987) studied 187 seizures in 14 infants less than 2
years old, with suspected partial epilepsy (of
temporal/extratemporal origin) and reported that behavioral arrest
and tonic, bilaterally symmetric extensor stiffening were the
commonest clinical manifestations seen in complex partial seizures
during infancy. Similar observations were reported by Acharya et
al. (1997). They analyzed 125 seizures in 23 infants aged 2-24
months, with “localization-related epilepsy” (again of temporal or
extratemporal origin), with seizure-free outcome after resective
surgery. Localization-related epilepsy was defined as either a
localized ictal EEG or a localized lesion on neuroimaging. They
concluded that seizure symptomatology could be divided into the
following broad categories; the first characterized by behavioral
arrest and decreased motor activity (hypomotor), which arose from
temporal, temporo-parietal or occipital regions (7 patients), and
the other with predominantly motor (clonic, tonic or atonic)
manifestations, which arose predominantly from frontal,
fronto-parietal, central or frontocentral regions (12 patients).
They also classified a 3rd major category, i.e.
epileptic spasms, which could arise from either location.
In a more detailed, subsequent study (Hamer et al. 1999), 296
videotaped seizures from 76 patients aged 1-35 months, with either
generalized or partial epilepsy were reviewed. The authors reported
that four clinical patterns accounted for 81% of all seizure types.
These were epileptic spasms (24%), clonic seizures (20%), tonic
seizures (17%) and hypomotor seizures (20%; defined as behavioral
arrest, cessation or significant decrease in motor activity with an
indeterminate level of consciousness). The Cleveland Clinic
epilepsy group (Acharya et al. 1997, Hamer et al. 1999) prefer the
use of the term “hypomotor”, since it emphasizes the cessation, or
the significant reduction of behavioral and/or motor activity
without committing to the level of consciousness, since this is
difficult to ascertain in very young children.
Other studies of TLE seizure in children revealed similar
observations. Fogarasi et al. (2002) analyzed 83 seizures in 15
children aged 11-70 months, selected by post-temporal lobectomy,
seizure-free outcome and found that there was a linear and inverse
correlation between the ratio of motor components with increasing
age. All children younger than 42 months had seizures with early
and marked motor features (tonic, myoclonic, spasms). These motor
components decreased with increasing age and, in fact, in 5/11
children older than three years, were completely absent.
Brockhaus and Elger (1995) studied 29 children with temporal
lobe seizures, aged 18 months to 16 years who experienced either
seizure-freedom or significant improvement in seizure control
following temporal lobectomy. They concluded that seizure semiology
in children > 6 years was similar to that in adults
including auras, psychomotor arrest, simple and complex
automatisms, versive movements and dystonic posturing. However, in
children younger than six years, typical seizure semiology included
symmetric motor phenomena of the limbs (up to 80%), more
reminiscent of frontal lobe seizures of adults. These motor
symptoms occur much less often (approximately 40%) in older
children. They also noted that automatisms become increasingly
complex with age. Whereas only simple automatisms such as
oroalimentary, gestural and blinking were seen in preschool
children, more complex automatisms such as hand clapping, beating
hands on a blanket or card shuffling were only seen in children
older than eight. None of the pre-school children (1-6 years) in
their series exhibited any complex automatisms compared to 4/4
children in the 13-16 years age group who had complex
automatisms.
Jayakar and Duchowny (1990) examined 126 seizures in 26 children
younger than 12 years, with unilateral TLE (in this case defined by
clear electrographic documentation of seizures of unilateral
temporal lobe onset on the basis of ictal EEG), and found
motionless staring, behavioral automatisms and motor activity to be
the commonest manifestations throughout childhood. While initial
motor activity was significantly more common in infants (28%),
staring at seizure onset was more frequently (90%) seen in the
school-age child. Automatisms were frequent (71%-88%) at all ages,
but their nature and complexity changed with age. Simple gross
motor and oro-alimentary automatisms were seen in infants and
pre-schoolers, fine motor acts, complex postures and axial
automatisms were more frequent in the school age child (75%).
Limitations of ictal semiology
Oller-Daurella and Oller (1989) emphasized the importance of
recognizing patients with partial (temporal and extratemporal)
epilepsy presenting initially with a non-partial ictal semiology.
They identified 154 cases of partial epilepsy in the first 3 years
of life. Of these, only 35 (23%) patients had partial seizures
(simple or complex partial or secondarily generalized tonic-clonic
seizures) as their initial seizure manifestation, while non-partial
seizures were the initial manifestation in 119 (77%) patients.
Generalized (tonic, clonic, tonic-clonic, myoclonic or atonic)
seizures were the initial manifestion in 62 (40%) patients. Also,
of these 119 patients with non-partial initial manifestations, 31
patients showed a seizure-free interval of several years between
the initial presentation and the subsequent occurrence of partial
epilepsy, raising the possibility of misdiagnosis based on the
initial seizure type alone. Their conclusion was that partial
epilepsy may be misdiagnosed in the first 3 years of life, either
because of the lack of partial features in the ictal semiology or
the young age of the child precluding reporting of subjective
phenomena during the initial part of the ictus (e.g. aura). Other
studies (Dravet et al. 1989, Yamamoto et al. 1987) emphasized the
limitations of the role played by ictal semiology in infants, in
determining the localization-related nature of an epileptic
seizure.
Case studies
We present some illustrative cases of children with a diagnosis of
TLE as defined by clinical semiology, EEG findings, neuroimaging,
as well as seizure-freedom/significant improvement after temporal
lobectomy.
Case 1
A 4-year-old, right handed male with medically intractable epilepsy
whose seizures began at 2 years of age. In the video, after the
child’s face is turned towards the camera, he lies still without
much response or movement. This seizure would be classified as
hypomotor in the Cleveland Clinic Classification scheme. Facial
automatisms are mentioned by the nurses, although they are not
clearly seen on the video. The prominent motor manifestations seen
in infants are not seen with increasing age, especially in
school-age children. The EEG showed focal spikes, and seizure
origin from the left temporal region. The MRI of this patient ((
figure 1 ))
showed a left temporal lobe lesion (tumor versus dysplasia) and a
PET scan showed left temporal hypometabolism. He had a left
temporal lobectomy and a follow-up of 3 years during which he
remained seizure-free. Pathology revealed cortical dysplasia.
Case 2
A 2 1/2-year-old male who started having seizures when he was one
year old. In the video, note the extensive motor manifestations
that the child exhibits that are more reminiscent of frontal lobe
seizures; this is often the case in infants and pre-school children
with TLE. Contrast this seizure with the relative paucity of motor
symptomatology in Cases 1, 3 and 4. This patient’s MRI showed a
right temporal lobe tumor. He underwent resection of this tumor and
remains seizure-free 12 years after surgery. Pathology suggested a
protoplasmic astrocytoma (with coexistence of meningioma, in a
single piece of the resection).
Case 3
A 13-month-old female who started having seizures at nine months
old. In the video, after the child puts down the bottle, notice the
paucity of motor manifestations. This is another example of a
hypomotor seizure where it is difficult to establish any alteration
of consciousness. Therefore, it becomes difficult to classify the
seizure as simple or complex partial using the ILAE seizure
classification system. In the later part of the seizure, notice the
simple nature of the oral automatisms, which are characteristic of
this age group. With increasing age these become more elaborate and
complex. The MRI of this patient (( figure 2 )) showed a left
temporal lobe tumor, which had been partially resected at another
insitution (without benefit). The patient underwent further
resection of the tumor and has since remained seizure-free and
tumor-free 7 years after surgery. Pathology showed a
ganglioglioma.
Case 4
A 3-year-old boy who started having seizures at the age of 13
months. Initially, seizures were reported as myoclonic jerks of the
limbs with occasional head drops. However, over the course of time
they evolved to the current semiology as shown in the video. As in
the previous case, note the behavioral arrest with a paucity of
motor features during the initial part of the seizure, followed by
the simple mouth automatisms seen later in the video. The MRI ((
figure 3 )) was
suggestive of right temporal lesion (dysplasia versus tumor). PET
showed hypometabolism of right temporal region. He underwent
resection of the lesion, along with right temporal lobectomy.
Pathology was consistent with cortical dysplasia. He was
seizure-free at last follow-up, 6 months after surgery.
Case 5
The salient features in the video of this 6-year-old, left-handed
girl who started having seizures at the age of two years include
the initial cry, which probably represents an aura of fear probably
in response to a visual hallucination (she reported seeing monsters
on some occasions and robbers on other occasions). She displays
fine distal automatisms of the left upper extremity, along with
dystonic posturing of the right upper extremity (similar to TLE
semiology characteristic of adults and older children), with
lateralization and localization to the left temporal lobe. EEG
showed left temporal spikes and seizure onset. The MRI scan ((
figure 4 ))
showed a cystic lesion in the left mesial temporal region. She
underwent left temporal lobectomy along with tumor resection.
Pathology was suggestive of ganglioglioma. She was seizure-free at
last follow-up, six months after surgery.
Case 6
This 5 1/2-year-old, right-handed girl presented with an episode of
status epilepticus at 15 months of age. Her current seizure type
began at 3 ½ years of age and these would occur 2-4 times per
month. After arousing from sleep, in this video she displays
discrete automatisms of the distal right upper extremity, including
fumbling around with the blanket. This is in contrast to the coarse
and simple automatisms exhibited by the younger patients in Cases 3
and 4. EEG showed spikes and seizures from the left temporal
region. The MRI (( figure 5 )) showed volume
loss and increased signal in the left hippocampus. PET showed
marked left temporal hypometabolism. She underwent a left temporal
lobectomy and remains seizure-free 3 ½ years after surgery.
Pathology was suggestive of hippocampal sclerosis
Case 7
This 4 1/2-year-old, right-handed boy presented with status
epilepticus at the age of nine months. His present seizure type
(see video sequence) begins with an abdominal aura. The abdominal
aura is followed by dystonic posturing of the right hand,
behavioral arrest, inability to speak and bilateral, fine upper
extremity automatisms. These features suggest a left temporal lobe
seizure-onset, as confirmed by focal spikes and seizures noted on
EEG from this region. The MRI of the brain revealed evidence of
volume loss as well as a signal abnormality in the left
hippocampus. PET scan showed hypometabolism of the left temporal
region. He had a left temporal lobectomy and remains seizure-free 3
½ years post-surgery. Pathology revealed evidence of hippocampal
sclerosis as well as a cortical dysplasia.
Case 8
An 18-year-old, left-handed male who started having seizures at the
age of 10 months. In the video he wakes up from sleep and tries to
press the seizure button. This is followed by a phase during which
he just lies in bed experiencing some subtle, fine automatisms.
Next we see tonic pulling of the right side of the face along with
head deviation to the left followed within seconds by a generalized
tonic-clonic seizure. This type of sustained, involuntary,
unnatural and forceful head deviation is classified as a versive
seizure and when closely followed (within 10 seconds) by a
generalized tonic-clonic seizure, lateralizes seizure focus to the
contralateral hemisphere (Ochs et al. 1984, Wyllie et al. 1986,
Kernan et al. 1993, Fakhoury and Abou Khalil 1995, Marks and Laxer
1998), in this case the right. The patient’s EEG showed evidence of
slowing, and seizure onset from the right temporal region. The MRI
revealed a right temporal malformation of cortical development ((
figure 6 )). The
patient underwent a right temporal resection and has been
seizure-free for 16 months. Pathology was suggestive of focal
cortical dysplasia.
Case 9
This 16-year-old, right-handed female started having seizures at
the age of 12 years. She has an aura of fear and déjà vu
followed by profound oral and hand automatisms along with some
difficulty with speech, although she is able to produce purposeful
speech. The EEG localized seizure onset to the left temporal
region. The MRI (( figure 7 )) revealed a
possible hamartoma in the left temporal region. Interestingly, the
WADA test lateralized speech to the left hemisphere. She had
invasive monitoring followed by left temporal lobectomy and remains
seizure-free one year after surgery. Pathology revealed focal
cortical dysplasia.
Case 10
This video is illustrative of how temporal lobe seizures may
occasionally present with atypical features. This 8-year-old boy
had gelastic seizures (usually associated with hypothalamic
hamartomas), with spikes, and seizure-onset (after invasive
recordings with subdural electrodes) from the left temporal region.
MRI revealed possible subtle malformation in the left anterior
temporal region. He remains seizure-free seven months after left
temporal resection. Pathology revealed focal cortical dysplasia.
Conclusion
To summarize, TLE in infants and young children is often due to
etiologies other than mesial temporal sclerosis, namely
developmental low-grade tumors and malformations of cortical
development. Differences in seizure semiology are also noticeable.
In infants, motor manifestations are prominent; with increasing
age, these become less evident. Although automatisms are also seen
in young children with TLE, they are simpler and less elaborate.
Oral automatisms are more common compared to manual automatisms.
With age, automatisms tend to become more discrete and complex. It
is also important to remember that very young children with partial
epilepsy (including TLE) may present with initial manifestations
which are non-partial or generalized in character (such as
epileptic spasms) and could be misdiagnosed as generalized
epilepsy. This has profound implications for the pre-surgical
evaluation since epilepsy surgery may render these hitherto
“non-surgical candidates” seizure-free.
The salient features of TLE syndromes presenting at different
ages are summarized in table 1, highlighting the differences
between the childhood and the adult syndromes.
Acknowledgements
Thanks are due to Adina Chirla and Najla Najeeullah for helping
with the collection of data, and to Angela Fleischman for help with
the videos.
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