Brain Advance Access originally published online on July 13, 2005
Brain 2005 128(12):2822-2829; doi:10.1093/brain/awh597
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Greater functional recovery after temporal lobe epilepsy surgery in children
1 Department of Epileptology and 2 Department of Neurosurgery, University of Bonn, Bonn, Germany
Correspondence to: Ulrike Gleissner Ph.D., Department of Epileptology, University of Bonn, Sigmund-Freud Strasse 25, 53105 Bonn, Germany E-mail: ulrike.gleissner{at}ukb.uni-bonn.de
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Summary |
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The purpose of our study is to evaluate whether children recover better than adults from memory deficits as a consequence of temporal lobe surgery. We compared 3 and 12 month outcomes obtained in children and adults with medically refractory epilepsy. Each candidate underwent temporal lobe resection for seizure control and children were matched with regard to pathology, onset of epilepsy, side of surgery and type of surgery with adults (N = 30 for each group, mean age at surgery 13 versus 30 years). Three months after surgery, both left-resected groups displayed a significant decline in verbal learning capacity. During the following 9 months, only the children recovered and were able to reach their preoperative level 1 year after surgery. The left-resected adults remained, for the most part, on their low level and one year after surgery, they were still significantly worse than at the time of their preoperative examination. The right-resected adults experienced a deterioration in visual memory 1 year after surgery relative to the results of the short-term follow-up; the children improved. The children also had a better outcome with regard to attentional functions and, as a trend, a better seizure outcome (Engel Outcome I—1 year after surgery: 63% adults, 80% paediatric patients). Our neuropsychological data provide evidence of greater plasticity and compensational capacity in childhood. The results can be taken as a strong argument for early surgical intervention.
Key Words: children; memory; surgery; temporal lobe epilepsy
Abbreviations: IQ = intelligence quotient; TLE = temporal lobe epilepsy
Received January 18, 2005. Revised April 14, 2005. Accepted June 23, 2005.
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Introduction |
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Resective surgery in children with medically intractable symptomatic epilepsy has been recognized as a viable treatment option for almost 30 years. Since severe intractable epilepsy may have a progressive, cumulative impact on cognitive and social development, it has been stated that early surgery performed to cure epilepsy is beneficial for those patients who are suitable surgical candidates. Longitudinal studies reported that no intellectual decline occurred when children responded well to drug treatment (Bourgeois et al., 1983
; Ellenberg et al., 1986). However, persistent seizures in childhood probably slow down the rate of cognitive and psychological development (Hirsch et al., 2000; Oguni et al., 2000). Children with a longer duration of an active epilepsy are reported to have lower intelligence quotients (IQs) than those children with a shorter seizure history (Farwell et al., 1985; Robinson et al., 2000). Bjornaes et al. (2001) recently reported evidence that the long-term effects of intractable seizures are more serious in children than in adults.
Children usually tolerate surgery well and their outcome with regard to seizures is at least as good as those results reported in adults (Wyllie et al., 1991; Clusmann et al., 2004). After temporal lobe resection 
70% of the patients can expect to become seizure free compared with a rate of 60% for those patients who have undergone frontal lobe surgery (Guenot, 2004; Kral et al., 2001). Studies concentrating on the cognitive outcome after temporal lobe surgery in paediatric patients are comparatively rare. A comprehensive review of available studies has recently been provided by Lah (2004). Group outcome studies on intelligence in paediatric patients provided little evidence of significant changes after temporal lobe resections, and if a change occurred, it was an increase, not a decrease, in IQ (Lewis et al., 1996; Miranda and Smith, 2001; Westerveld et al., 2000). Recently, we compared pre-operative and post-operative verbal memory performance in 55 children and adolescents with temporal lobe epilepsy (TLE) (Gleissner et al., 2002). Post-operative verbal memory declines were observed 3 months after surgery and these declines were associated with a left-sided resection and a higher pre-operative performance. However, recoveries were evident just 1 year after surgery. A comparable post-operative course in memory with a significant decline followed by a relatively fast and efficient recovery has not been observed in adults. On the contrary, stability of deficits over time has been reported in adult patients after short (Gleissner et al., 2004) and even after very long retest intervals (Rausch et al., 2003).
Studies that have included mainly adult patients reported a better neuropsychological outcome associated with a younger age at the time of surgery and a shorter duration of TLE (Helmstaedter and Elger, 1996, 1998; Hermann et al., 1995). Table 1 provides an overview of those studies that have reported memory outcome by using standardized tests in patients who underwent temporal lobe resections as children. The results are not unequivocal. Some studies observed a decline in memory while others did not report any significant changes after surgery. In summary, studies that have found no evidence of post-operative decline (8 of 14) are more frequent than studies that revealed a loss (5 of 14) (for a more elaborative review and discussion of existing studies in this field, see Lah, 2004). This suggests that compared with adults, children may be less vulnerable to memory decline after surgery. However, it is extremely difficult to compare children and adults presented in different studies, because the samples often differ with respect to clinical features. It has been stated that TLE in childhood may constitute a different entity than in adults, from both the clinical and neuropathological perspectives (Bocti et al., 2003). For instance, several studies have reported that cortical dysplasia and benign tumours are common findings in children with TLE, but mesial temporal/hippocampal sclerosis is relatively rare (Wyllie et al., 1998). Therefore, in the present study we directly compared a group of children with adults, who were matched not only with regard to the pathology, but also with regard to the onset of epilepsy, the side of surgery and largely also to the type of surgery. This approach is unique and was possible only because of our large database. To our knowledge, there is no other study using a similar selection procedure. Our goal was to simulate a situation in which similar patients had been operated on as children or as adults and thus to evaluate the outcome with respect to seizures and neuropsychological measures in otherwise largely comparable groups.
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Patients
We searched our database for adult patients with temporal lobe resections (age at surgery >20 years) who corresponded exactly to those paediatric patients described in our previous study (N = 55, age at surgery <18 years) with regard to side of surgery, onset of epilepsy (±4 years) and pathology and, in most cases also, the type of surgery. In some cases, it proved difficult to find equivalent adult patients because only few patients had the same pathology. In other cases, the patients had a later onset of epilepsy. We were finally able to locate in a pool of 483 adult and 55 paediatric temporal lobe resected patients 30 pairs who fulfilled the matching criteria. There were no significant group differences with respect to the onset of epilepsy (F = 1.1, P = 0.8); gender ratio (
2 = 0.6, P = 0.4); number of seizures (U = 310, P = 0.1); seizure types (2 < 0.7, P > 0.4); pathology (2 = 1.0, P = 1.0); side of surgery (2 = 0.0, P = 1.0); and type of surgery (2 = 0.7, P = 0.7). When children and adults were grouped according to the side of lesion, both groups showed no significant differences in the onset of epilepsy (F < 0.06, P > 0.8); gender ratio (2 < 0.9, P > 0.3); number of seizures (U > 29.4, P > 0.07); seizure type (2 < 0.9, P > 0.3); pathology (2 < 1.1, P = 1.0); and the type of surgery (2 < 059, P > 0.7). The range of age at surgery was 7–17 years in the paediatric group, and 21–46 years in the adult group (F = 177, P < 0.001). Patient characteristics are listed in Table 2. The old histological diagnoses were kept in the table and the modern classification by Palmini and Lüders (2002) is shown in the footnote. Please note, that the distribution of pathologies is not typical for adult patients since they were selected as pairs for the children. Usually, hippocampal sclerosis is the main pathology in adult patients with TLE who are candidates for surgical treatment. Handedness was evaluated with the Edinburgh Handedness Inventory (Oldfield, 1971). The questionnaire was completed with the help of the children's parents (when necessary). The groups displayed a significant difference in hand dominance (2 = 6.3, P = 0.04) with more right-handed patients being children. The paediatric group comprised mainly right-handers owing to the selection criteria outlined in our former study (Gleissner et al., 2002). Non-right-handers were included only when an intracarotid amobarbital test had confirmed unilateral language dominance of the left hemisphere. The purpose of this selection was to exclude those patients with atypical language dominance because they are assumed to differ markedly with regard to their functional memory organization, even if they are children (Gleissner et al., 2003). Therefore, they should be evaluated separately.
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Neuropsychological assessment
All patients underwent a neuropsychological examination to determine memory, attention, language and visuo-spatial functions pre-operatively, and at 3- and 12-month intervals after surgery.
Verbal memory was assessed with parallel test versions of the Verbal Learning and Memory Test (Helmstaedter et al., 2000), a standardized German version of the Auditory Verbal Learning Test (AVLT) by Rey, which allows assessment of several parameters. It requires learning a word list of 15 unrelated concrete words in five consecutive trials, free recall after learning an interference list, delayed free recall and recognition after 30 min. The parameters of interest were learning capacity (total number of words across all five learning trials) and loss after delay (number of words in trial 5 minus number of words in delayed free recall), since these parameters have been shown to reflect preferential involvement of neocortical and mesial temporal structures (Helmstaedter et al., 1997). The test results were standardized (T-values, mean 50, SD 10) according to normative data supplied in the handbook.
Visual memory was assessed by parallel test versions of a revised version of the ‘Diagnosticum für Zerebralschädigung’, the DCS-R (Helmstaedter et al., 1991a,b), which requires repeated learning of nine abstract designs each consisting of five lines in six consecutive trials. After each trial the patient has to reconstruct the designs with five wooden sticks retaining the spatial orientation. The parameter of interest was the learning capacity (total number of correct figures across all five learning trials). The test results of children were standardized (T-values, mean 50, SD 10) according to normative data of 91 healthy controls (age range 6 to 16 years) collected in an unpublished doctoral dissertation (Willmes, 2000). The test results of adults were standardized (T-values) according to the normative data of 102 healthy controls (mean age 29.8, SD 8.8) collected in our hospital (published in parts in Helmstaedter et al., 1991b).
We were able to use specific memory test parameters, because memory tests were the same in children and adults and the choice of memory tests has remained the same over the years. Attentional, language and visuo-spatial functions were assessed in children of different ages and in adults with a slightly heterogeneous test battery and the test repertoire was modified over the years. Table 3 provides a survey of the test battery, listing the tests in a cumulative manner, e.g. the Trail-Making Test is given to patients of all ages. We used a general classification system instead of separate test scores in order to allow a direct comparison among age groups and different tests applied for a certain domain. The general classification included the categories ‘0 = strongly impaired’, ‘1 = impaired’, ‘2 = borderline’, ‘3 = average’, and ‘4 = above average’. Classification into categories is routinely accomplished by the psychologist who conducts the examination. A domain is rated as strongly impaired when at least one measure of the same skill is significantly below average (T-value < 30). Impairment is concluded when at least one measure of the respective domain is below average (T-value < 38) and the criteria for the category ‘borderline’ are not fulfilled. The category ‘borderline’ is used if at least two measures are in the borderline range (T-value between 38 and 42) or when one measure below average (T-value < 38) is outweighed by otherwise average or above average results. The category ‘average’ is used if all measures are in the average range (T-value between 42 and 58) or if only one measure is within the borderline range (T-value between 38 and 42). The category ‘above average’ requires at least one measure to be above average (T-value > 60).
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Intelligence was assessed by a standardized test in 53 patients. In the remaining patients, school attendance or graduation in a mainstream school served as indications of normal or near normal intelligence. In adults, intelligence was assessed in 27 patients by administering a vocabulary test: ‘MWT-B’ (Lehrl, 1978
). This test is similar to the widely used NART test (Nelson, 1978). In the paediatric group, eight adolescent patients were assessed by the MWT-B, eight patients were assessed by Raven's Standard Progressive Matrices (SPM) and ten were assessed by a German version of the Wechsler intelligence test for children (HAWIK-R; Tewes, 1983 and HAWIK-III; Tewes et al., 1999). Groups differed significantly in the intellectual level with the paediatric group showing lower scores (Table 2, F = 7.4, P = 0.009). When the IQs of children and adults were evaluated separately and categorized according to the side of epilepsy, the difference was almost significant for patients with right TLE (F = 3.5, P = 0.07) and significant for patients with left TLE (F = 5.1, P = 0.03). Within the groups, the side of epilepsy had no significant effect on IQ (F < 2.8, P > 0.12). |
Results |
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Seizure outcome
Seizure outcome was dichotomized based on the Engel Classification Grade 1 as ‘seizure free’ and ‘not seizure free’. No significant differences were reported in seizure outcome between groups 3 months (
2 = 0.8, P = 0.4) or 1 year after surgery (2 = 2.1, P = 0.1). In the paediatric group, 80% (24 of 30) were seizure free 3 months and 1 year after surgery. In adults, 70% (21 of 30) were seizure free at the short-term follow-up and 63.3% (19 of 30) were seizure free 1 year after surgery.
Cognitive outcome
Pre-operative and post-operative memory scores are provided in Table 4 separately for left-resected and right-resected patients. First, we performed univariate repeated measurement analyses with ‘Group’ (adult versus child) and ‘Side of surgery’ (left versus right) as independent factors, memory parameter as dependent measure and the three levels of ‘Time of examination’ (pre-operative, 3 months post-operative and 1 year post-operative) as repetition factor. The results indicated significant two-way interactions between ‘Time of examination’ and ‘Group’ for verbal learning capacity (F = 3.2, P = 0.049) and visual learning capacity (F = 3.8, P = 0.029), and between ‘Time of examination’ and ‘Side of surgery’ for verbal learning capacity (F = 4.7, P = 0.014) and loss in delayed recall (F = 3.7, P = 0.031). There was a significant three-way interaction of ‘Time of examination’, ‘Group’ and ‘Side of surgery’ for visual learning capacity (F = 3.2, P = 0.05). We then evaluated the ways in which the groups changed by separate analyses from
- pre-operative to 3 months post-operative,
- three months to one year post-operative,
- pre-operative to 1 year post-operative.
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Analyses I (pre-operative to 3 months post-operative) showed a significant interaction of ‘Time of examination’ and ‘Side of surgery’ for verbal learning capacity (F = 9.5, P = 0.003). Left-resected patients experienced a decline while performance was stable in right-resected patients. There was no interaction of ‘Time of examination’ and ‘Group’ indicating that both children and adults with left- sided resections showed a decline in verbal memory in the short-term follow-up.
Analyses II (3 months to 1 year post-operative) indicated a two-way interaction of the factors ‘Time of examination’ and ‘Group’ in verbal learning capacity (F = 4.0, P = 0.05) that was due to a recovery of performance in children 1 year after surgery, while the adults remained on their performance level of 3 months after surgery. A three-way interaction was evident between ‘Time of examination’, ‘Side of epilepsy’ and ‘Group’ for visual learning capacity (F = 6.5, P = 0.01). The right-resected adults tended to experience visual memory deterioration 1 year after surgery, while children tended to improve. In the left-resected groups, both adults and children showed no changes over time. The two-way interaction between ‘Time of examination’ and ‘Group’ was also significant (F = 5.2, P = 0.02), owing to a positive trend in children and a negative trend in adults.
Analyses III (pre-operative to 1 year post-operative) indicated interactions of ‘Time of examination’ and ‘Group’ (F = 5.7, P = 0.02) and of ‘Time of examination’ and ‘Side of surgery’ (F = 4.5, P = 0.04) in verbal learning capacity. Children displayed no changes 1 year after surgery when compared with their pre-operative level, while declines were observed in adults, particularly if the resections were on the left side.
In all analyses (I, II and III) the factor ‘Group’ had a significant main effect on verbal memory owing to the children's superior performance (all F > 4.8 with P < 0.03). The factor ‘Side of surgery’ had a significant main effect on verbal memory owing to lower performance in those patients with left TLE (all F > 4.1 with P < 0.04). Significant effects of ‘Time of examination’ were evident for verbal memory in analyses I and III (all F > 4.1 with P < 0.049) indicating a post-operative change. There were no significant main effects of ‘Group’, ‘Side of surgery’ and ‘Time of examination’ for visual memory (all F < 1.8 with P > 0.18) indicating that no global changes occurred after surgery in visual memory.
To examine whether seizure outcome (seizure free versus ongoing seizures), type of resection (anterior temporal lobectomy or lesionectomy including the hippocampus versus other resections), pathology (benign tumour, neuronal migration disorder, other finding), hand dominance (right versus not right) and pre-operative intelligence level had a significant impact on the post-operative development, we calculated difference scores (post-operative minus pre-operative score) for the memory parameters and computed ANOVAs and Pearson correlations. Patients who were not seizure free had as a trend a stronger decline in visual memory 1 year after surgery (F = 3.7, P = 0.059). All other results were not significant (F < 3.0, P > 0.057; r < 0.17, P > 0.21).
Table 5 shows the percentage of patients with either gains or losses in attention, language or visuo-spatial functions defined very conservatively as a category difference 
2. To evaluate whether the observed proportions of changes are statistically significant, we calculated binomial tests assuming, based on the 90% confidence interval, that a change in either direction (gain or loss) should occur by chance in 5% of the cases. The binomial tests indicated that the attentional gains in children 1 year after surgery occurred more often than can be expected by chance independent of the side of surgery (P < 0.015). For right-resected children, the number of losses in visuo-spatial functions 3 months after surgery was significantly higher than expected (P < 0.001). However, 1 year after surgery, there was only a small number of right-resected patients who experienced losses in visuo-spatial functions (P > 0.3). These changes were not related to the post-operative seizure situation (2 < 0.9 with P > 0.3). In order to evaluate possible relationships between changes in memory and other functions (attention, language and visuo-spatial functions), we calculated non-parametric correlations (Spearman, Bonferroni-adjusted significance level 0.05/3 = 0.017) between the corresponding difference scores (post-operative minus pre-operative score). In general, changes in language were associated positively with changes in verbal learning capacity (3 months after surgery: r = 0.27, P = 0.02). All other correlations were not significant (all r < 0.21 with P > 0.06).
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Discussion |
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We compared patients with epilepsy who were matched according to their pathology, side of surgery, type of surgery and onset of epilepsy; one group underwent surgery as children, the other as adults. This study design is unique; it guarantees a comparison of similar patient groups. Our results indicated worse verbal memory performance in patients with left-sided epilepsy. This is a stable finding in adults. In the present study, it was true for both paediatric and adult patients when we used combined pre-operative and post-operative values. Pre-operatively, adults with left temporal epilepsy scored lower than children in verbal memory probably owing to the longer duration of epilepsy in adults. This was particularly evident for a parameter that is known to reflect mesial temporal functioning, the loss of words after a time delay (Helmstaedter et al., 1997
). In both left-resected groups, verbal learning capacity significantly declined 3 months after surgery. Only the children recovered during the following 9 months and reached their pre-operative level 1 year after surgery. Adults largely remained on their low level and, 1 year after surgery, they were still significantly worse than in the pre-operative examination. Right-resected adults deteriorated in visual memory 1 year after surgery relative to their results of the short-term follow-up; the children with right-sided resection improved between the 3 and 12 month follow-up assessments. No significant effects were observed for seizure outcome, hand dominance, pre-operative intellectual level and type of resection on the post-operative memory outcome. Our paediatric group had lower pre-operative IQ levels than the adult group. This presents a paradoxical situation in our study. When compared with adult patients, the paediatric patients with TLE had a higher level of memory but lower IQ scores. This may be owing to methodological differences. When evaluating children, we applied mostly long and sophisticated tests; all of the adults were assessed with a shorter test that mainly relied on verbal crystallized intelligence. In any case, the IQ difference cannot account for the different post-operative development of children and adults. Compensatory capacities are considered to be worse in patients with a lower intellectual level and hence those patients usually are expected to be more at risk for post-operative declines. Based on the difference in intelligence, we would thus have expected exactly converse results with the children being at a disadvantage. Children, however, also had a better outcome regarding attentional functions, in which a significant number of patients improved 1 year after surgery. Right-resected children had a significant number of decreases in visuo-spatial functions at the short-term follow-up, but this was no longer evident 1 year after surgery. Changes in these non-memory functions were not related to the changes in memory functions. Children had as a trend a better seizure outcome. One year after surgery, 80% children but only 63% adults were seizure free (Engel Grade I).
We can conclude from our results that early surgery in patients with symptomatic epilepsy is beneficial because the seizure outcome was at least as good and neuropsychological outcome was better in children than in adults. It should be kept in mind, however, that the distribution of pathologies—only one patient in each group had Ammon's horn sclerosis—was not typical for adults. Hippocampal sclerosis is usually the main pathology found in adults with TLE. Thus, our results cannot be generalized for adults with TLE. Also, our results cannot be generalized for children with TLE because our selection criteria excluded those patients with atypical language dominance. Hence, our results are valid only for those patients in whom a typical left-sided language dominance can be assumed. Another limiting factor of the present study is the relatively short post-operative retest interval. Most of our paediatric patients were still children or adolescents at the post-operative examination and we cannot completely rule out the possibility of a ‘growth into a deficit’ during the subsequent development. A study by Lindsay et al. (1984a) followed surgically treated paediatric patients with TLE into adulthood. This study indicated a better psychosocial outcome of temporal resected patients compared with non-surgical patients. Most of the patients who were treated surgically during childhood were well integrated and employed as adults. In another study, Lindsay et al. (1984b) found that global gains often took several years to be achieved. These early results indicate a positive long-term development after epilepsy surgery in paediatric patients. However, there is an urgent need for more research concerning the long-term consequences of epilepsy surgery in children.
The different post-operative course in adults and children in the present study is most likely owing to the age difference between groups with one group still being in the brain development phase because the groups were matched with regard to other potentially important clinical and aetiological variables. The recoveries in children 1 year after surgery are probably owing to the plasticity in the immature brain. Plasticity is defined as the brain's capacity to be shaped by experience, its capacity to learn and remember and its ability to reorganize and recover after injury. Recovery after unilateral motor cortex lesions in experimental animal research (Kennard, 1942) and language development in children with early left hemispheric damage and hemispherectomy (Boatman et al., 1999) show an increased plasticity in the immature brain. For instance, left hemisphere damage sustained during early childhood usually does not produce long-lasting aphasia, if the homologous areas on the right are functional. The restitution of functions is thus often faster and more complete following a focal injury that occurs during childhood. Ongoing maturation of the temporal lobes during the second decade of life is indicated by electroencephalographic studies, post-mortem studies and MRI studies (Buchsbaum et al., 1992; Benes et al., 1994; Giedd, 2004). These processes of brain development extending until puberty may enable children and adolescents to experience a post-operative recovery after epilepsy surgery that is no longer possible in adults.
On the other hand, the immature brain may be particularly vulnerable to a negative influence of recurrent seizures. The brain develops according to a correlation principle; connections between neurones that fire together are strengthened and, in the long run, only the active synapses survive. Epileptic activity could mix-up this selection principle by blurring the meaningful activity with meaningless epileptic activity. It has been shown, that patients with early cerebral damage show much stronger deficits if the damage is accompanied by seizures than if it is not (Vargha-Khadem et al., 1992). It would appear as though the epilepsy itself has a negative effect on cognitive development. Seizures starting in childhood that are due to known structural lesions and are not controlled with first-line and second-line drugs are unlikely to remit as the child grows older. Therefore, when a symptomatic epilepsy starts during childhood, early surgical intervention can be recommended to allow for an optimal brain development.
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