revue neurologique 171 (2015) 252–258

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Hippocampus and epilepsy

Temporal lobe epilepsy in infants and children E´pilepsie temporale chez le nourrisson et l’enfant S. Gataullina a,*,b,c, O. Dulac a,b, C. Bulteau a,b a

INSERM U1129 ‘‘Infantile Epilepsies and Brain Plasticity’’, service de neurope´diatrie, hoˆpital Necker-Enfants Malades, baˆtiment Lavoisier, 149, rue de Se`vres, 75015 Paris, France b Neurophysiologique clinique, hoˆpital Mignot – Le Chesnay, 177, rue de Versailles, 78150 Le Chesnay, France c Neurochirurgie pe´diatrique, fondation ophtalmologique Rothschild, 25, rue Manin, 75019 Paris, France

info article

abstract

Article history:

Clinical expression of temporal lobe seizures is different with a more diverse and more

Received 2 December 2014

extensive etiology in infants and children than it is in adults. It is dominated by cortical

Received in revised form

dysplasia, low-grade tumors and perinatal damage. Hippocampal sclerosis, although less

17 January 2015

frequent, exists in children usually as a dual pathology associated with ipsilateral neocor-

Accepted 27 January 2015

tical lesions. The clinical semiology of temporal seizures is more varied, and sometimes

Available online 2 March 2015

misleading. Motor features including tonic, clonic or myoclonic behaviors, and infantile spasms predominate in infants. Classical complex partial seizures with behavioral arrest

Keywords:

and automatisms, as well as lateralizing signs are rare and occur mostly with onset after the

Temporal epilepsy

age of two years. Interestingly, aura, emotional, and autonomic signs seem to be indepen-

Infant

dent on the brain maturation process. Moreover, the neuropsychological profile varies

Child

according to age of onset and duration, lateralization of the focus and etiology. Quality

Infantile spasms

of care benefits from individual cognitive assessment for memory and emotional processes. # 2015 Elsevier Masson SAS. All rights reserved.

Dysplasia Mots cle´s : E´pilepsie temporale Nourrisson Enfant Spasmes infantiles Dysplasie

r e´ s u m e´ L’expression clinique des crises temporales varie selon l’e´tiologie, laquelle est plus varie´e chez l’enfant que chez l’adulte, domine´e par les dysplasies, les tumeurs de bas grade et les le´sions acquises. La se´miologie temporale classique concerne les petites dysplasies ou` l’e´pilepsie de´bute dans l’enfance. Lorsqu’elle de´bute plus toˆt, chez le nourrisson, les symptoˆmes sont plus souvent moteurs, pouvant re´aliser des spasmes infantiles. L’impre´cision des limites de la dysplasie demande un enregistrement intracraˆnien, de pre´fe´rence par ste´re´oe´lectroence´phalographie, pour l’approche chirurgicale. Les tumeurs de bas grade, souvent associe´es a` une dysplasie, demandent aussi un enregistrement intracraˆnien, en particulier pour une dysembryoplasie neuroe´pithe´liale. Les autres types de tumeurs (angiocentrique, gangliogliome, me´ningiomatose, hamartome) sont plus rares. Un cavernome, voire un ane´vrysme arte´rio-veineux sont souvent une de´couverte de l’imagerie. Les le´sions

* Corresponding author. E-mail address: [email protected] (S. Gataullina). http://dx.doi.org/10.1016/j.neurol.2015.01.559 0035-3787/# 2015 Elsevier Masson SAS. All rights reserved.

revue neurologique 171 (2015) 252–258

253

clastiques (ische´mo-he´morragie, inflammation, se´quelles d’e´tat de mal convulsif) de´bordent habituellement le lobe temporal, voire l’he´misphe`re entier, et le risque d’e´pilepsie est particulie`rement important en cas d’inflammation ou d’infiltration d’he´moside´rine. La se´miologie est alors enrichie d’e´le´ments extratemporaux, les spasmes sont relativement fre´quents. La pharmacore´sistance conduit a` envisager une chirurgie qui se limite rarement a` une re´section temporale et l’implication de la re´gion motrice avec un de´ficit moteur ame`ne a` proposer une de´connexion he´misphe´rique. Bien que la scle´rose hippocampique soit moins fre´quente que chez l’adulte, elle existe chez l’enfant, habituellement comme double pathologie associe´e a` des le´sions du ne´ocortex ipsilate´ral. Une crise fe´brile prolonge´e, souvent unilate´rale, survenue dans les premie`res anne´es de vie, peut eˆtre un facteur favorisant sur une le´sion pre´existante. Des cas d’association a` une mutation du ge`ne SCN1A sont identifie´s lorsque l’histoire clinique est celui d’un syndrome de Dravet. Un foyer poste´rieur peut orienter vers une mutation dans PCDH19. La se´miologie des crises temporales est variable et parfois trompeuse. Les crises partielles complexes classiques avec arreˆt de l’activite´ et automatismes, ainsi que les signes de late´ralisation surviennent surtout apre`s l’aˆge de 2 ans. Les manifestations motrices sont toniques, cloniques ou myocloniques, et les spasmes infantiles pre´dominent chez le nourrisson. Il est remarquable que les signes e´motionnels et autonomiques, et les auras soient inde´pendants de la maturation ce´re´brale. Un retard mental et des troubles psychiatriques peuvent compliquer une e´pilepsie pre´coce et pharmacore´sistante. L’e´pilepsie temporale de l’enfant s’accompagne souvent des troubles cognitivo-e´motionnels. Si la chirurgie permet de gue´rir les crises et atte´nuer le retentissement neuropsychologique, des de´ficits mne´siques peuvent persister a` long terme et doivent eˆtre de´cele´s et pris en charge. # 2015 Elsevier Masson SAS. Tous droits re´serve´s.

In contrast to adults in which mesial temporal lobe epilepsy (MTLE) is considered a common and well-delineated condition, mesial and neocortical temporal epilepsies can hardly be distinguished in childhood and even less in infancy. Etiology of temporal lobe epilepsy is diverse, dominated by cortical dysplasia and perinatal damage; although hippocampal sclerosis is far from being rare, it is often combined with cortical lesions. Determining the extent of the epileptogenic zone is often a challenge, particularly when inflammatory or vascular etiology is involved, but also for dysplasia. Etiology determines clinical expression of the epilepsy. Furthermore, the younger the child, the most clinical semiology has motor and bilateral expression, including clusters of infantile spasms, and very misleading is the total lack of seizures which may characterize the condition described by Landau and Kleffner. Therefore, particularities of clinical expression and comorbidity factors according to etiology in children with temporal lobe epilepsy need to be considered.

1.

Focal cortical dysplasia

Focal cortical dysplasia (FCD) is the most frequent cause of temporal lobe epilepsy [1,2]. Over half the cases of pharmacoresistant epilepsy result from FCD that can result from abnormal multiplication or migration of neuroblasts, or from abnormal intracortical organization; therefore, isolated cortical dyslamination (type I) or the combination of dyslamination, dysmorphic neurons and columnar disorganization (type II) may be present, while the combination of FCD with additional pathology (for example, FCD and hippocampal sclerosis) is labeled ‘‘type III’’ [3,4].

Ictal semiology depends partly of the extent of the dysplasia, the least extensive causing onset in childhood with loss of contact, eventually automatisms similar to those of adults. However, in young children, motor manifestations, particularly limb jerks, express extension of the discharge to the neocortex. EEG may show major focal paroxysmal activity in the temporal region when the neocortex is involved. MRI shows disappearance of the normal white matter indentations compared to the contralateral side that is particularly visible in T2 coronal sequence [5]. The posterior limits of the lesion are difficult to determine. Positron emission tomography mildly improves disclosure of the lesion and of its limits, since the most challenging cases have major interictal paroxysmal activity that tends to reduce the metabolic gradient between the lesion and the healthy tissue, thereby making the lesion difficult to see. Most challenging is the onset in the first 2 years of life with infantile spasms and/or tonic seizures, eventually atypical absences with diffuse paroxysmal anomalies consisting either of hypsarrhythmia or of slow spike-waves. MRI in cases with such early onset often shows that the whole hemisphere is smaller than the contralateral one although the abnormal signal of the white matter only affects the temporal lobe, expressing that the abnormality seen on the MRI and appearing clearly as a dysplastic lesion is only the ‘‘tip of the iceberg’’ [6]. Antiepileptic drugs (AED) are poorly efficient although vigabatrin may be helpful, namely when infantile spasms occur. In pharmacoresistant cases, surgery should aim at removing the whole epileptogenic zone that usually corresponds to the malformation itself. In cases of beginning early with infantile spasms or tonic seizures with lesion located in

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temporal lobe, intracranial recording may be indicated particularly when the left side is involved in order to define the ictal discharges of all seizure types and spare the functional cortex. Intracranial EEG guides tailored resection that contributes to improve long-term cognitive development [7,8]. This procedure is however far from being the rule.

2.

Tumors

Tumors are the second most frequent cause. Ictal expression is determined by the location and age of onset of seizures. Paradoxically, tumors that have mild or no growing potential are the most epileptogenic. They are often surrounded by dysplastic tissue, and in this case their precise limits are often difficult to determine on MRI. It is even pharmacoresistant epilepsy that in two instances – dysembryoplastic neuroepiltelial tumor (DNET) [9] and angiocentric neuroepithelial tumor (ANET) [10–12] – pointed to the biological particularities of such tumors: mild growth contrasting with major epileptogenicity. As for other areas of the brain, DNET and ANET in the temporal lobe are combined with a cortical dysplasia in over 3/ 4 of the cases [13,14]. It was well shown for DNET that resection of all the abnormal tissue is required to ensure seizure control. Chassoux et al. [15] proposed optimal resections for the three histologic subtypes based on MRI features. Even ganglioglioma, the most frequent epileptogenic tumor with tendency to grow, usually concerns extra-temporal localization [16]. However, it is pleomorphic xanthoastrocytoma due to BRAF mutation that has the highest tendency to grow, likely due to a predominant glial component [17–19]. At the opposite, meningoangiomatosis is a non-growing hamartoma, but diagnosis cannot be done before histology, and surgery is therefore indicated, even if seizures are under control [20]. Indeed, various combinations of cystic and calcic modifications, ferritine accumulation and gliosis characterize these different tumors. Tumor removal should include healthy peritumoral tissue. Intracranial recording is indicated if the tumor is located near eloquent tissue. Only the rare aggressive forms of pleomorphic xanthoastrocytoma require additional oncological treatment – chemo- or even radiotherapy.

3. Ischemic-hemorrhagic (porencephaly and encephalomalacia) damage and stroke-like (hemiconvulsion-hemiplegia syndrome) lesions Ischemic-hemorrhagic (porencephaly and encephalomalacia) damage and stroke-like (hemiconvulsion-hemiplegia syndrome) lesions are rarely restricted to the temporal lobe, they usually extend to the whole hemisphere, or to 2 homologous lobes, or even both hemispheres [21]; however, as shown in surgical cases, seizure symptoms correlate with mesial temporal origin but not with the cyst location [22]. Although vascular causes (infarct or hematoma – maternal thrombopenia, intraparenchymal hemorrhage of the premature, trauma or COL4 mutation) are the most frequent clastic lesions, viral (herpetic encephalitis), bacterial (meningitis, abscess) or parasitic (cysticercosis, malaria) infections, trauma and severe hypoglycemia (namely when associated with

infection or hypoxia-ischemia) of metabolic (hyperinsulinism, b-oxidation trouble, glycogen storage disease) or iatrogenic (administration of excessive doses of insulin) origin may also cause cystic necrosis or/and epileptogenic gliosis. The acute phase producing the lesion usually comprises repeat convulsive seizures with loss of consciousness. Epilepsy is often delayed for a few months to several years, especially following neonatal damage. Epilepsy affects over half the cases, and the risk is particularly high in case of cortical infiltration with hemosiderin (following hemorrhage) or of inflammatory (following herpetic encephalitis) component of the lesion. However, following early acute damage, temporal epilepsy is less frequent than infantile spasms namely because the damage is rarely restricted to one hemisphere. Ictal semiology of temporal lobe seizures following acute damage depends of the topography and extent of the lesion, and of the age of the first seizures [23]. It may, namely when the lesion occurred after the neonatal period, consist of infantile spasms beginning often after the age of one year of life. When seizures begin after the age of 3 years and the lesion is limited to a single lobe seizures are usually focal. Ipsilateral hippocampal sclerosis and atrophy of the amygdala are present in most cases [22]. The identification of the epileptogenic zone is often challenging since it tends to be widespread, involving also the contralateral hemisphere and not only limited to damaged areas of the brain, sometimes across eloquent areas that cannot be removed without causing a deficit. Invasive EEG monitoring directing multilobar resections is necessary in many cases [21,24]. In addition, if one epileptogenic area is particularly active, others less active ones could become leaders once the most active one has been removed. Surgery is therefore difficult in this context. In order to determine the extent of the cortex to be removed, intracranial recording is usually required. Even if semiology is consistent with pure mesial temporal involvement, additional neocortical involvement should be suspected, realizing a dual pathology that requires more extensive removal than only that of mesial structures [25]. If destruction involves the perisylvien area including the corticospinal pathway, hemispheric disconnexion is sometimes the most appropriate indication [26,27]. In such children with pre-operative contralateral hemiparesis, partial seizures originate from areas surrounding the porencephaly, far from the temporal lobe. Post-operatively, although seizure freedom improves gross motor function and walking, finger independence is lost and the child as his parents must be aware beforehand of such future deficit. However, children who have lost finger movements in the pre-operative state, experience no post-operative deterioration. Speech will improve even if it is affected transiently following the procedure. Hemianopsia is not reversible but usually does not affect the quality of life enough to disqualify such procedure. Sometimes ‘‘uncapping’’ is possible, removing the gliotic cortex that lies over a porencephaly [28]. It is however preferable to avoid opening the porencephaly into the ventricle because of the hydrodynamic troubles that may result [24]. Whatever the kind of surgical treatment, surgery should be performed as soon as possible to optimize functional brain reorganization [24,27].

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4.

Hippocampal sclerosis

Hippocampal sclerosis (HS) is considered to be less frequent in children than it is in adults. However, it exists also in children as ‘‘dual pathology’’ and is associated with neocortical lesions involving ipsilateral temporal convexity or pole (FCD or lowgrade tumor) [2,25,29]. Extrahippocampal pathology should be suspected in infants who start seizures before the age of 6 years. In addition, seizures at an early age (younger than 6 months) are less likely to cause seizure-induced hippocampal injury [30]. When HS is combined with ischemic or infectious lesions, mechanism is uncertain: the hippocampus belongs to a vascularisation area that is fragile because it is at the junction of sylvian and posterior arterials areas; hippocampal deafferentation from necrosed neocortex is also considered. A story of complicated febrile seizures (HHV6 is occasionally disclosed from the CSF) is classical and several reports mention transitory post-ictal edema of mesial structures followed by atrophy and sclerosis [31]. In addition, HHV6 is disclosed from hippocampal samples in 50% of patients with MTLE [32–34]. Genetic predisposition may contribute to complicated febrile seizures [35]. Recurring temporal seizures may then progressively worsen the sclerosis and the atrophy. However, such anamnesis is often missing and the cause of the sclerosis remains unknown, a perinatal lesion or a mild malformation being difficult to confirm. After a prolonged seizure eventually febrile in the second semester or second year of life, focal epilepsy with clusters of seizures triggered by fever in a girl with temporo-occipital focus should indicate the possibility of a mutation in the PCDH19 gene [36]. The combination of hippocampal sclerosis with a history of Dravet syndrome and a mutation in SCN1A has also been reported [37] although this is a rare event [38]. HS in this context raises difficult issues for therapy that can only be solved on the basis of very strict anatomo-electro-clinical analysis.

5.

Cavernoma

Cavernoma is the most frequent vascular epileptogenic lesion involving temporal or frontal lobes [39]. Childhood cavernomas are larger in size than adult one, and may have cystic changes. When cavernomas are familial due to mutations in CCM1, -2 or -3, they are more often multiple than single and infratentorial than temporal, and carry a higher risk of hemorrhage [40]. Free radicals and hemosiderin deposit in the surrounding cortex due to micro-hemorrhages (whereas macroscopic hemorrhages are rarer) contribute to the longstanding epilepsy. A T2* MRI sequence is more likely to identify it than angiography since cavernoma is poorly vascularised. Electrocorticography from the cortex around the cavernoma has shown continuous spiking similar to the pattern shown in dysplastic cortex [41]. If surgery is undertaken, removal of the vascular lesion alone is usually sufficient although seizure freedom may require excision of the hemosiderin capsule and surrounding brain. Since 20% of patients with cavernoma have additional lesions, temporal lobe cavernoma requires that dual pathology with mesial temporal sclerosis be excluded [41,42].

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Arterio-venous aneurysms (AVA) raise similar issues. Epilepsy seldom begins in infancy, more often in childhood. The risk of hemorrhage is particularly high when the AVA is located in the cortex, which is the case when it is epileptogenic, reinforcing the indication for removal. Sturge-Weber disease is often suspected at birth faced to an extensive congenital port-wine stain angioma, permitting to begin preventive antiepileptic treatment [43]. However, the latter does not permit to prevent the first seizures to occur between 3 and 6 months of life as long lasting unilateral clonic jerks, followed by prolonged motor defect. Epilepsy itself begins several months later as partial seizures with frequent motor component. Infantile spasms are rare. HS following prolonged unilateral seizure may occur, particularly in the context of fever. Carbamazepine may be helpful. Surgery should be indicated before psychomotor delay develops. Intracranial recording that would be technically difficult because of the risk of hemorrhage is usually not indicated because the limits of the lesion are straightforward.

6.

Diversity of the electro-clinical expression

The classical semiology of mesial temporal seizures is rarely observed in infants. Children younger than three to four years present mostly motor features with tonic, clonic or myoclonic components, or even infantile spasms; beyond this age, complex partial seizures with behavioral arrest and automatisms become predominant [23]. Automatisms, secondary generalization and a number of different lateralizing signs increase with age, whereas aura, emotional, and autonomic signs are independent of the brain maturation process [44]. Infantile spasms, isolated or combined with focal seizures may be the main expression when epilepsy begins before the age of 2 years; later and up to 5 years of age late-onset spasms may be the revealing expression [45]. Tonic seizures may be combined when epileptic spasms begun after the age of one year, which is usually the case for temporal lesions. EEG is usually hypsasrrhythmic but asymmetrical and sometimes relatively synchronous on both hemispheres, expressing that myelination is already well developed. The pattern may consist of a combination of West and Lennox-Gastaut syndromes, with clusters of spasms and tonic seizure, slow spike-waves and interictal spikes predominating in the temporal areas. Such syndromes comprise cognitive troubles that indicate urgent treatment. When present, focal seizures indicate the epileptogenic zone, and therefore surgery gives better results when both seizure types are combined than when there are only infantile spasms. In addition, there may be contralateral spikes, particularly if there is an extensive temporal lesion or when the lesion is mesial, but this should not contra-indicate surgery [46,47]. The most misleading electro-clinical expression of temporal epilepsy is Landau-Kleffner syndrome that combines epilepsy and aphasia (usually of perception) and auditory agnosia, with continuous spike-waves during slow sleep (CSWS) involving both temporal regions, therefore as long as spikes are not controlled, recovery of speech is not possible [48]. On the other hand, control of the spike activity permits the child to start learning speech, which requires many

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months. Some children have two types of temporal epilepsy successively: following febrile seizure, the child develops aphasia and CSWS. Many months after the control of CSWS, he develops mesial temporal epilepsy resulting from the prolonged febrile seizure that occurred several years earlier that had caused hippocampal sclerosis.

7.

Neuropsychological considerations

Deficit of memory functions is often unrecognized in children with TLE [49–51]. Imperfect memory consciousness [52] and greater dependency on the family may explain why in young children this deficit often goes underreported or may lead to only minor complaints. Memory disorders affect however daily life and school learning in school-age children and adolescents with TLE [53]. Families report the feeling that working and helping them in their lessons is like writing in the sand meaning that the child forgets at school the homework he learnt the day before. Limitations in episodic memory with respect to side of the focus have been demonstrated for a long time [54,55]. They can be difficult to identify before the age of 5 or 6 years as evidenced in patients with developmental amnesia [56]. Recognition of a different pattern of memory deficit in respectively left or right TLE requires specific neuropsychological tools including verbal and visual episodic memory items [55]. The pitfall is to consider the epileptic child as having no specific cognitive deficit since his intellectual quotient appears normal in the absence of proper assessment of episodic memory performance, which is implicated in school learning [57]. Another possible origin of memory deficit in children with TLE is the relationship between episodic memory and emotion since the amygdalo-hippocampus complex is involved in both functions [58]. The enhancement of memory abilities by emotional memory processes is less efficient in children with refractory TLE [59]. The implication of the amygdala in the recognition of facial expressions of emotion is intimately related to the mesiotemporal memory network. Depending on the etiology and the duration of the seizure disorder, TLE in children may affect progressive functional maturation of the different amygdala nuclei that takes place from childhood to adolescence in healthy children [60]. This could explain the differences between adults and children. Children with TLE experience deficit in emotional facial expression, mainly fear and disgust with the exception of fearful faces expressions. The deficit involves familiarity rather than recollection as is the case in healthy individuals [61]. In addition, psychopathology, namely disorders of mood and personality, hyperactivity, social difficulties including autistic-like behavior has been reported [62]. While the majority of children with TLE keep normal intellectual abilities, early onset of seizures is a deleterious factor for intelligence and social abilities and a possible cause of mental retardation and psychiatric disorders in refractory epilepsy [63,64]. Together, these findings indicate that children with refractory temporal lobe epilepsy are candidates for presurgical neuropsychological evaluation. Globally, surgical TL resection has good prognosis for seizure freedom and for

academic and social development but the long-term effect on memory trajectory remains a challenge in children [65–68]. The beneficial effects of surgery on memory functions, particularly on material-specific memory, are difficult to assess because of potentially interacting factors such as age range, intellectual level, left-handedness, type of surgery and seizure outcome. Improvement of some memory scores is related to seizure freedom and brain plasticity, which facilitate post surgical reorganization [69]. Finally, children with TLE may be cured from seizures by surgery but not completely normalized for memory functions and require careful long-term assessment [8]. Therefore, etiology of temporal epilepsy is more diverse in children than it is in adults, and epileptogenic lesions tend to be more extensive in children, often overflowing into neighboring lobes. Electro-clinical semiology is therefore more varied, and sometimes misleading. MRI may show subtle signs, and it is not sure that increasing the number of teslas will raise the chances of seeing the lesion and its limits. PET can only have limited contribution. As temporal lobe is crucial for children to develop normal interactions between emotions and memory, neuropsychological assessment including memory and emotional processes are helpful to determine the implication and the lateralization of the mesiotemporal structures. For FCD, it seems to be the identification of clinico(spasms, tonic seizures) electro- (hypsarrhythmia and eventually slow spike-waves) MRI- (blurring of the temporal white matter combined with subtle hypoplasia of the rest of the hemisphere) anatomical (type I FCD) syndromes that will permit improving therapeutic choices. Identifying neurophysiological bases of epileptogenesis should open new therapeutic avenues permitting to reduce the indications of surgery or the extent of the resection and finally also enhance neuropsychological development.

Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

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Temporal lobe epilepsy in infants and children.

Clinical expression of temporal lobe seizures is different with a more diverse and more extensive etiology in infants and children than it is in adult...
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