Brain Advance Access originally published online on April 13, 2005
Brain 2005 128(7):1536-1545; doi:10.1093/brain/awh499
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Epilepsy surgery does not harm motor performance of children and adolescents
1 Department of Paediatric Physical Therapy and Exercise Physiology, 2 Department of Neuropsychology, 3 Department of Paediatric Rehabilitation, 4 Department of General and Special Education, Utrecht University, 5 Department of Child Neurology, University Medical Centre, Wilhelmina Children's Hospital and 6 Rudolf Magnus Institute of Neuroscience, Utrecht, The Netherlands
Correspondence to: R. van Empelen, NetChild, Department of Paediatric Physical Therapy and Exercise Physiology, University Medical Centre, Wilhelmina Children's Hospital, RM. KB 02.056.0, P.O. Box 85090 3508 AB, Utrecht, The Netherlands. Network for Childhood Disability Research in The Netherlands E-mail: R.vanEmpelen{at}wkz.azu.nl
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Summary |
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The impact of epilepsy surgery on motor performance, activities of daily life (ADL) and caregiver assistance was assessed in 37 children (age range 0.1–15.4 years) with pharmacologically untreatable epilepsy, 17 of whom were also diagnosed as having spasticity of cerebral origin. All patients underwent epilepsy surgery between 1996 and 2001 at the Wilhelmina University Children's Hospital and were assessed using a standard protocol at fixed intervals: before surgery and 6 months, 1 year and 2 years after surgery. The type of surgery was hemispherectomy (n = 14) and temporal (n = 14), frontal (n = 4), parietal (n = 2) and central (n = 2) resection. One child underwent callosotomy. Engel's classification was used to determine seizure outcome. Impairments were measured in terms of muscle strength, range of motion and muscle tone. Motor performance of infants and children without spasticity was measured using the Movement Assessment Battery for Children (M-ABC). The Gross Motor Function Measure (GMFM-88) was used in children with spasticity, the severity of motor disability in this group being determined by means of the Gross Motor Function Classification System (GMFCS). Daily activities and caregiver's assistance were measured in all children using the Pediatric Evaluation of Disability Inventory (PEDI). Twenty-four months after surgery 74% of the children could be classified as Engel class 1, indicating a significant seizure reduction. Impairments revealed some decrease in muscle strength and range of motion in the group with spasticity. Scores improved statistically significantly at group level on M-ABC and GMFM (P < 0.05). Improvement in activities of daily life and caregiver's assistance could not be measured in children without spasticity because of the ceiling effect of the PEDI, but children with spasticity improved significantly with respect to these parameters (PEDI) (P < 0.05). Hence, epilepsy surgery does not harm motor performance in children with or without spasticity.
Key Words: epilepsy surgery; children; motor development; GMFCS; activities of daily life (ADL)
Abbreviations: ADL = activities of daily life; GMFCS = Gross Motor Function Classification System; GMFM = Gross Motor Function Measure; ICF = International Classification of Functioning, Disability and Health; M-ABC = Movement Assessment Battery for Children; PEDI = Pediatric Evaluation of Disability Inventory
Received October 11, 2004. Revised March 6, 2005. Accepted March 7, 2005.
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Introduction |
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Epilepsy surgery has become a prominent intervention for children and adolescents with pharmacologically untreatable epilepsy (Wyllie et al., 1998
; Graveline et al., 2000; Devlin et al., 2003). Favourable effects on seizure outcome have been reported for different types of surgery (L. S. Chen et al., 2002; Devlin et al., 2003) and psychosocial benefits of surgery have become clear (Lendt et al., 2000; Birbeck et al., 2002; Ronen et al., 2003a, b; Smith et al., 2004).
One of the criteria for resective surgery is interference of seizures with neurodevelopment (Peacock et al., 1993), but as yet there is no consensus on the outcome of this criterion. Reports on motor aspects of development after surgery are contradictory. Some researchers have described no deterioration and even an improvement in motor function, whether or not the epilepsy resulted in cessation or reduction of seizures (Beckung et al., 1994; Romanelli et al., 2001; Krsek et al., 2002). Others found motor deterioration to be a frequent complication of epilepsy surgery (Chassoux et al., 1999; Graveline et al., 1999). In order to provide children and parents with better information on the impact of surgery, there is a need for evaluation to be carried out systematically. Moreover, the impact of epilepsy surgery on activities of daily life and caregiver's assistance (and, for that matter, independence) has to be taken into account. Covering the period from prior to epilepsy surgery up to the third year after the operation, our study focuses on change in motor performance, activities of daily life and in caregiver's assistance. The taxonomy of anatomical and physiological functions, activities and social participation offered by the International Classification of Functioning, Disability and Health (ICF) provided a useful guide for the present prospective, longitudinal study (World Health Organization, 2001). In a previous paper (Empelen et al., 2004) we reported that impairments were only slightly associated with functional outcome after hemispherectomy. We now report, at the individual level, a change in motor performance in two groups (children with and without spasticity) compared with reference data, and at group level a change in functional skills and caregiver assistance after various surgical procedures.
The fact that a subgroup of children had spasticity necessitated the use of different instruments, suitable for the assessment of motor performance. The Movement Assessment Battery for Children (M-ABC), designed to assess normal motor performance, was used for children without spasticity (Henderson and Sugden, 1992). For children with spasticity, the Gross Motor Function Measure (GMFM) was the instrument of choice (Russell et al., 2002). Classification of gross motor function has been performed with the Gross Motor Function Classification System (GMFCS) (Palisano et al., 1997).
Furthermore, we reasoned that seizure reduction might enhance independence and hence participation in social activities. Knowledge of the impact of epilepsy surgery on activities of daily life of children is as yet in an exploratory stage. Comparing daily functional activities in children who underwent hemispherectomy with candidates for this surgical procedure, Graveline and colleagues found no significant difference, although candidates for hemispherectomy tended to attain higher levels than children who had had surgery (Graveline et al., 2000). However, our own data on hemispherectomized children suggested that, after surgery, there was an improvement in the performance of daily activities and in independence (Empelen et al., 2004). In order to help solve this controversy, we describe a wider range of children in this study.
The present study applies the novel concept of stratifying motor growth according to level of gross motor function (GMFCS) (Rosenbaum et al., 2002) to the changes found in the subgroup of surgically treated children with spasticity of cerebral origin. We drafted these motor growth curves using the data as described by Russell and colleagues on the GMFM-88 at each level of the GMFCS (Russell et al., 2002).
The study addresses two questions: (i) does epilepsy surgery of children with pre-existing neurological deficit (spasticity) worsen motor impairments or harm motor performance, and what are the effects of epilepsy surgery on activities of daily life and caregiver assistance in these children? (ii) does epilepsy surgery of children without pre-existing neurological deficit cause motor impairments, worsen or improve motor performance, and what are the effects of epilepsy surgery on activities of daily life and caregiver assistance in these children?
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Methods |
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Participants
Thirty-seven children (15 male, 22 female) who underwent surgery for pharmacologically untreatable epilepsy at the Wilhelmina Children's Hospital in the period 1996–2001 were the subjects of the present study. Median age at surgery was 8.6 years (range 0.1–15.4). Exclusion criteria were age older than 16 years at the time of surgery and the presence of a progressive neurometabolic disease. Patients were assessed using a standard protocol with fixed intervals: before surgery, and 6 months, 1 year and 2 years after surgery.
Fourteen children underwent hemispherectomy. Fourteen children underwent temporal, four frontal, two parietal and two central resection. One child underwent callosotomy. For the sake of conciseness, the demographic and illness variables are presented separately for children without spasticity (Table 1) and for children with spasticity (Table 2) together with the major motor results and the outcome with respect to seizures. Prior to surgery, 17 children had spasticity of cerebral origin. In these children gross motor function was classified with the GMFCS (see Instruments): level 1 (n = 6); level 2 (n = 4); level 3 (n = 2); level 4 (n = 2); level 5 (n = 1); two children were too young to be classified. Eight of the 17 children had a non-progressive encephalopathy known as cerebral palsy; the aetiologies were congenital middle cerebral artery infarction (n = 3), hemiplegia, hemiconvulsions, epilepsy syndrome (HHE; n = 1), hemimegalencephaly (n = 3) and cortical dysplasia (n = 1). The remaining nine children with spasticity had progressive encephalopathies; the aetiologies were Rasmussen encephalitis (n = 4), Sturge–Weber syndrome (n = 2) and cerebral tumour (n = 2). In one child a callosotomy was performed; aetiology of the epilepsy remained unclear (Table 2).
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Instruments
Seizures: Engel's classification of postoperative outcome
Seizure frequency was determined using the modified classification of Engel and colleagues (Engel et al., 1993
): class 1 = free from seizures or residual auras; class 2 = child experienced intermittent, infrequent seizures or relapsed after a significant seizure-free period; class 3 = worthwhile improvement (>75% reduction in seizure frequency). Children who experienced less than 75% reduction in seizure frequency were classified as Engel class 4. Engel's classification was applied 24 months after surgery by the same child neurologist (O.v.N.).
Motor impairments
We assessed muscle strength, range of motion and muscle tone as relevant parameters.
Muscle strength of the extremities was assessed proximally and distally and scored according to the criteria for manual muscle testing, using the six-point scale (MRC range 5–0) (Medical Research Council, 1943; Hislop and Montgomery, 2002).
Range of motion was measured using the Joint Alignment and Motion (JAM) scale, a five-point scale of motion decrease (0 = no decrease, 1 = 1–5%, 2 = 6–25%, 3 = 26–75% and 4 = 76–100% decrease) (Spiegel et al., 1987).
Muscle tone was assessed using the Modified Ashworth Scale (MAS) (Bohannon and Smith, 1987), a six-point scale of tone increase [0 = no resistance; 1 = slight catch when limb is moved; 1+ = slight increase in muscle tone, manifested by a catch, followed by minimal resistance throughout the remainder (less than half) of the range of motion; 2 = resistance in whole range of movement; 3 = strong increase with decreased range of movement; 4 = limb rigidly in flexion or extension] (Bohannon and Smith, 1987).
Motor performance: Movement Assessment Battery for Children
To measure the overall level of motor function and to screen for movement problems in children without spasticity, the M-ABC (Henderson and Sugden, 1992; Smits-Engelsman, 1998) was used. The M-ABC has been standardized for children from 4 to 12+ years. Children are set eight age-appropriate tasks (age band 1, 4–6 years; band 2, 7 and 8 years; band 3, 9 and 10 years; band 4, 11 years and older) that pertain to three domains: Manual Dexterity (three tasks), Ball Skills (two tasks) and Static and Dynamic Balance (three tasks). Six-point scale values (0–5) are summed (range 0–40) and the total score is converted into an age-related centile score, which is interpreted as ‘normal and good’ (100th to 16th centile), ‘at risk for motor problems’ (15th to 6th centile) and ‘impaired’ (5th centile and below) (Henderson and Sugden, 1992). The lower the raw scores the better the motor function and the higher the centile score. Test–retest reliability (0.75) and inter-rater reliability (0.70–0.89) of the Dutch version of the M-ABC are satisfactory (Smits-Engelsman, 1998).
Severity of motor disability: Gross Motor Function Classification System
The GMFCS manual provides separate descriptions for four age bands: before 2nd birthday, 2nd to 4th birthday, 4th to 6th birthday, 6 to 12 years. For each age band, mobility is classified into five levels; the title of each level represents the highest level of mobility that a child within that level is expected to achieve. For children over the age of 6 years, level 1 is described as ‘walks without restrictions, limitations in more advanced gross motor skills’, and level 5 is described as ‘self-mobility is severely limited even with the use of assisting technology’ (Palisano et al., 1997). The overall reliability of the GMFCS is 0.79 and increases when tracking starts at higher ages. Inter-rater reliability is 0.93 (Wood and Rosenbaum, 2000). Validity has been reported to be excellent (Rosenbaum et al., 2002; Gorter et al., 2004).
Motor capacity in children with spasticity: Gross Motor Function Measure
The GMFM is a standardized clinical observational instrument designed to evaluate change in gross motor activities in children with cerebral palsy. It assesses how much of an activity a child can accomplish rather than how well the activity is performed (Russell et al., 1993, 2002). The 88 items of the GMFM-88 (Russell et al., 2002) are grouped into five dimensions: lying and rolling (17 items), sitting (20 items), crawling and kneeling (14 items), standing (13 items), and walking, running and jumping (24 items). The items are scored on four-point ordinal scales (0 = cannot initiate; 1 = initiates, but completes less than 10%; 2 = partially completes item (11–99%); 3 = completes item independently). Calculated by means of the intraclass correlation coefficient, reliability values varied from 0.87 to 0.99 (Russell et al., 1993, 2002; Ketelaar et al., 2001). Scores are percentages for each of the five GMFM dimensions and a total GMFM-88 percentage score. Higher scores indicate better capacity.
Change on this instrument used to be interpreted intuitively, but we could appeal to recently published reference data for the motor development of children with cerebral palsy (Russell et al., 2002; Rosenbaum et al., 2002). As motor outcome is limited by severity of motor disability in children with cerebral palsy, motor disability is scored by means of the GMFCS into five levels based on differences in self-initiated movement, with particular emphasis on sitting and walking (Palisano et al., 2000; Gorter et al., 2004). We compared change in children with spasticity to that in a reference group of children with spasticity caused by cerebral palsy, by mapping, for every GMFCS level, the mean GMFM-88 total score on the corresponding GMFM reference value published in the GMFM manual (Russell et al., 2002: Table A4.2, page 206).
Evaluation of activities of daily life (ADL) and caregiver assistance: Pediatric Evaluation of Disability Inventory (PEDI)
The PEDI (Haley et al., 1992; Custers, 2001) is a structured parent's interview that assesses functional skills (capability) and caregiver assistance. It covers the domains of self-care (73 items), mobility (59 items) and social functioning (65 items). The scaled scores offer the opportunity to estimate skills in older children whose functional abilities lag behind those expected of 7.5-year-old healthy children (Feldman et al., 1990; Haley et al., 1992; Nichols and Case-Smith, 1996; Custers, 2001). We used the scaled scores. The PEDI is sensitive to changes over time. The internal consistency for PEDI scales has 
scores ranging from 0.95 to 0.99 and a mean standard error of measurement of 0.09 (Haley et al., 1992; Custers et al., 2002). The scaled scores estimate the skill in each domain (0 = no measurable functional skill; 100 = intact functional skill; 0 = complete caregiver assistance; 100 = no caregiver assistance).
The smallest change in PEDI score that is considered to be associated with a minimal but clinically important difference in skill ranges from 6 to 15 points (mean = 11.5, SD = 2.8) for all PEDI scales (Iyer et al., 2003).
All parents of the children and, if over 12 years of age, the children themselves gave informed written consent and the study was approved by the Institutional Review Board.
Motor and ADL functions of all children were assessed by the paediatric physical therapist (R.v.E.), who had been trained in administering and scoring the GMFM. Reliability, as assessed compared with a criterion tape after this training, was adequate (weighted 
> 0.80). Use of the GMFCS requires familiarity with the child and the GMFCS levels, but no formal training.
Data analysis
Changes in M-ABC, GMFM-88 and PEDI scores were analysed using analysis of variance (ANOVA) for repeated measures with time (before surgery and 6, 12 and 24 months after surgery) as within-subject factor, with post hoc testing to compare sessions and adjust for multiple comparisons using the least significant difference (LSD). A two-sided P-value of 0.05 or less was considered statistically significant. SPSS software version 11.01 was used.
The influences of variables such as age of onset of epilepsy, age at surgery, time between onset of epilepsy and surgery, aetiology, type of surgery and Engel classification on the changes in M-ABC and GMFM values compared with reference data were explored by a linear mixed model analysis (program R, the statistical software package R version 1.8.1). Because of the small number of participants, only two variables could be used per item. For example, epilepsy surgery was categorized into temporal resection versus non-temporal resection in the group without spasticity, and type of epilepsy surgery into hemispherectomy versus non-hemispherectomy in the group with spasticity.
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Results |
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Seizure frequency
Table 3 shows Engel's classification of postoperative outcome (Engel et al., 1993
) by type of surgery. Two years after surgery, 27 children (74%) had achieved complete seizure control, five (13%) children still had rare seizures and the remaining five (13%) showed a worthwhile reduction (>75%) in number of seizures.
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Motor impairments
Range values of muscle strength, range of motion and muscle tone before and after surgery are shown in Appendix 1 for both the group without (n = 20) and that with spasticity (n = 17) (individual data can be obtained from the first author). In the group without spasticity, two children (one child in whom the epilepsy focus was right frontal and the other right central) had a slight impairment in muscle strength (before and after surgery) and muscle tone (after surgery). In the group with spasticity, muscle strength, range of motion and muscle tone of the arm and leg were mildly to moderately impaired on the affected side, before as well as after surgery.
Motor activities
M-ABC (n = 20)
Motor performance of the 20 children without spasticity is shown in both raw scores and centile scores (Table 1). In 16 out of 20 children, centile scores before surgery were below 16, meaning they were at risk of motor problems; 4 out of 20 had normal scores before surgery and at all times after surgery. Fourteen of the 20 children attained normal centile scores at 12 and 24 months; eleven of these had been below the 16th centile before surgery. In six children [four of them with a tumour (children 6, 8, 12 and 20)], the centile scores remained below 16 at all times. In the two children (children 11 and 16) with some impairment, one had normal values on the M-ABC centile scores after surgery. The mean centile scores were: before surgery, 12.5 (SD 14.2); 6 months after surgery, 19.0 (SD 16.8); 12 months after surgery, 27.8 (SD 21.3); 24 months after surgery, 37.3 (SD 27.5).
ANOVA for repeated measures confirmed a statistically significant change from before surgery to 6 months after surgery (P = 0.002) and from 1 to 2 years after surgery (P = 0.01).
GMFCS (n = 17)
Table 2 shows demographic and illness characteristics of 17 patients with spasticity separately for those with progressive and non-progressive encephalopathy. GMFCS levels prior to and 24 months after surgery are presented. Fourteen of the 17 children remained at the presurgery level. Two children improved (IvB from 5 to 3 and LD from 3 to 2) and one child (DB) worsened (from 1 to 2).
GMFM-88 (n = 17)
The mean total scores on the GMFM were: before surgery, 53.8% (SD 36.3); 6 months after surgery, 51.2% (SD 31.6); 12 months after surgery, 62.1% (SD 29.5); and 24 months after surgery, 69.5% (SD 28.7). The ANOVA repeated measures revealed significant changes, i.e. improvements between 6 and 12 months after surgery (P < 0.01) and between 12 and 24 months after surgery (P < 0.01).
GMFM stratified by GMFCS level
The scores of the 17 children on the GMFM-88 were compared with the mean GMFM-88 score reported in the GMFM manual according to the GMFCS level and age. Before surgery, 10 out of 17 children obtained scores that were more than 1 SD worse than their reference values, at 24 months after surgery six out of 17 children differed by more than 1 SD (three by +1 SD and three by –1 SD) and 16 out of 17 children scored within 2 SD of the mean referent score at that age band and GMFCS level (Table 4).
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Mixed linear model analyses showed variables such as age at onset of epilepsy, age at surgery, time between onset of epilepsy and surgery, aetiology, type of surgery, and the result of the Engel classification to have had no statistically significant effect on M-ABC and GMFM scores. Time after surgery, however, had a statistically significant effect on GMFM (P = 0.007) and M-ABC (P = 0.0001).
ADL and caregiver assistance
In Table 5, mean PEDI scores are presented for children with spasticity. One child with spasticity was younger than 0.5 years of age before surgery, while in another case the PEDI forms had not been properly completed 12 months after surgery.
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Due to a ceiling effect, change in ADL and caregiver assistance in children without spasticity remained unclear (data not shown).
In children with spasticity, the statistically significant effect of time in the ANOVA for repeated measure indicates that self-care [F(1.36) = 4.28, P < 0.05], mobility [F(2.44) = 6.96, P < 0.01] and social functioning [F(1.62) = 14.92, P < 0.001] improved at follow-up. Improvement appeared to be significant between 6 and 12 months and between 12 and 24 months after surgery in self-care, mobility and social functioning (all P values < 0.05).
Similarly, the statistically significant effect of time with respect to caregiver assistance indicates that assistance decreased in self-care [F(2.44) = 8.78, P < 0.001], mobility [F(1.44) = 6.13, P < 0.01] and social functioning [F(1.89) = 6.60, P < 0.01]. In other words, the children's independence increased. Improvement was statistically significant between 6 and 12 months and between 12 and 24 months after surgery (for all three dimensions P < 0.05).
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Discussion |
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Epilepsy surgery and motor function
Motor impairments and delays in motor development often coexist in childhood epilepsy (Beckung and Uvebrant, 1993
, 1997; Carlsson et al., 2003). This is not surprising, as motor activity depends, among other factors, on the integrity of the central nervous system as well as on the mood, concentration and motivation of the child. In terms of the WHO ICF (World Health Organization, 2001), motor impairments are usually due to the underlying cause of the epilepsy, i.e. a central nervous system lesion, or to the epilepsy itself, the medication or a combination of these factors (Carlsson et al., 2003). After successful epilepsy surgery, seizure reduction may reflect a better neurological state, which may allow the children access to a more effective motor system. This may be expressed in improved motor activity (Beckung et al., 1994), a view that seems to be confirmed by the present study. Notwithstanding the remaining impairments after surgery, especially in the group of children with spasticity, our study shows improvement of motor activity in the majority of the children, in whichever group. One should take note of the fact that most children in the group without spasticity (14 out of 20) were classified as normal at 24 months of follow-up, while at baseline 15 out of 20 were classified as being at risk of motor problems. In six children the centile scores remained below 16 at all times. Four of these children had a tumour (Table 2; children 6, 8, 12 and 20) and three of them still had epilepsy after surgery (one with Engel 3 and two Engel 2). Two children (child 7, with MTS, and child 16, with cortical dysplasia) had no seizures after surgery but motor activity remained retarded.
Beckung and colleagues reported a positive correlation between a favourable effect of surgery on seizures and improvement in motor activity (Beckung et al., 1994). They reported on different types of surgery (i.e. hemispherectomies, lobectomies, callosotomies) in a heterogeneous group of patients (children with and without spasticity); our data are in this sense comparable with those of Beckung and colleagues (1994).
Factors explaining change in motor activity after epilepsy surgery
Østensjo and colleagues recently reported on the basis of a study of 95 children with spasticity due to cerebral palsy a moderate relationship of spasticity, range of motion, selective dorsiflexion of the ankle (impairments) and gross motor function as measured with the GMFM (activities) (Østensjo et al., 2004). In a study of hemispherectomized children (Empelen et al., 2004), we also found that impairments were only slightly associated with functional outcome. It is therefore essential to measure not only the impairments (ICF domain of anatomical and physiological functions) but also motor activity (ICF domain: activities) in relation to epilepsy surgery and to be aware of differences in impairments and activities. The Engel score, as a result of reduced seizure frequency, is not related to the difference in results in the GMFM and M-ABC values. This is not surprising, as the Engel score is just one of the many components and factors that can influence motor and ADL functioning. Overall, we have to realize that impairments are not directly related to motor activity and daily functional activities.
Type of surgery, age at seizure onset, aetiology (congenital or acquired epilepsy), interval between age at seizure onset and time of surgery, and age at surgery are among the variables that have been suggested to be significant prognostic factors regarding the child's motor outcome (Graveline et al., 1999). However, we found no significant influence of these variables on GMFM and M-ABC results. We were interested to find out whether motor activity would improve more in younger children and children who were operated on at a younger age than in older children, because plasticity is thought to be age-dependent (R. Chen et al., 2002). We found only time after surgery to be significantly related to motor outcome.
GMFCS and GMFM
To our knowledge, this is the first study comparing motor activity in children with spasticity before and after epilepsy surgery with reference GMFM-88 scores as described in the GMFM manual by Russell and colleagues (Russell et al., 2002). They described developmental values derived from assessing children with cerebral palsy according to GMFCS level by age. We assessed the GMFCS level before and after surgery, and found changes in level scores in three children. In 14 out of 17, the GMFCS level remained stable from before the last postsurgery measurement time point. Changes in GMFCS level are rare in children with cerebral palsy (Rosenbaum et al., 2002). However, as in our children, GMFCS levels are also influenced by the epilepsy; therefore, changes in GMFCS level may be more likely than in the general cerebral palsy population to be due to improved seizure control after surgery. We compared our data on the GMFM-88 total score for each child before surgery and after surgery with the reference data according to GMFCS level. Twenty-four months after surgery, 16 out of 17 children scored within 2 SD of the expected score. Hence, the concept of GMFCS growth curves would seem to be useful when determining whether the child is performing in accordance with her/his expected growth curve of gross motor development. At least after surgery the growth curves can help to predict motor development in children with spasticity of cerebral origin. Our data suggest that children do not deteriorate in motor activity after epilepsy surgery. This finding is important, considering the uncertainties of parents and children about motor function after surgery.
ADL and caregiver assistance
The age ranges of the children with spasticity and of those without spasticity are quite different. This has consequences for the interpretation of PEDI scores. In the PEDI, norm scores are based upon the assumption that healthy children of 7.5 years of age score 100% in all domains. In the children with spasticity participating in this study, the median age was 6.1 years (range 0.3–15.4). Most of these children would, therefore, not reach a score of 100%, even without physical limitations. In the children without spasticity the median age was 11.5 (range 6.1–15.4). It is obvious that this group approached the 100% score very closely, because most of them were older than 7.5 and they did not have, except for their epilepsy, the concrete physical limitations which children with spasticity have. Clinically important changes in functional skills and caregiver assistance range from 6 to 15 points (Iyer et al., 2003). In our study, in children with spasticity the scores for functional skills and caregiver assistance on the PEDI increased from presurgery: 48.9–58.6 to 55.8–63.1, two years after surgery, indicating a clinically relevant improvement.
Limitations of the study
Our study has some intrinsic limitations. The changes in ADL function and caregiver assistance could not be detected in children without spasticity due to a ceiling effect of the PEDI instrument. For measuring changes in ADL function and independence in children aged 7.5 years and older with (severe) epilepsy and minimal physical limitations, a measuring instrument other than the PEDI should be available. The ceiling effect does not mean that there is no improvement in children without spasticity, but we were not able to measure this effectively.
The sample of children who participated in the present study is considered to be representative of the population of children with pharmacologically untreatable epilepsy who are eligible for epilepsy surgery and who have also been described in other studies (Devlin et al., 2003; Smith et al., 2004). The number of children in our study is, however, small; therefore, we have to be careful in the interpretation of the exploration of variables that may have influenced the results on GMFM and M-ABC scores. This study does not allow a detailed analysis of determinants of outcome, due to the small number of children and their heterogeneity in age, pathology and level of functioning.
In conclusion, 2 years after epilepsy surgery the motor function of most children develops in conformity with the expected motor development of children with and without spasticity, while impairments do not deteriorate. Caregiver's assistance decreases, indicating an increase in activities of daily functioning, in other words in the child's independence.
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Appendix I |
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Acknowledgements |
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We are grateful to the Phelps Stichting and the Johanna Children's Foundation for financial support, to Dr W. R. Pestman and Dr M. Schipper, Centre for Biostatistics, for supervision of the statistical analyses, and to E. van der Steeg, University Utrecht, Faculty of Social Sciences, for assistance in this research. The surgeons Prof. Dr C. W. M. van Veelen and Dr P. C. van Rijen operated on all patients. We thank the Members of the Dutch Collaborative Epilepsy Surgery Programme: SEIN, Kempenhaeghe, Hans Bergerkliniek, University Hospitals (Utrecht, Maastricht, Amsterdam VU).
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References |
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TopSummaryIntroductionMethodsResultsDiscussionAppendix IReferences |
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Beckung E, Uvebrant P. Motor and sensory impairments in children with intractable epilepsy. Epilepsia 1993; 34: 924–9.[CrossRef][ISI][Medline]
Beckung E, Uvebrant P. Hidden dysfunction in childhood epilepsy. Dev Med Child Neurol 1997; 39: 72–8.[ISI][Medline]
Beckung E, Uvebrant P, Hedström A, Rydenhag B. The effects of epilepsy surgery on the sensorimotor function of children. Dev Med Child Neurol 1994; 36: 893–901.[ISI][Medline]
Birbeck GL, Hays RD, Cui X, Vickrey BG. Seizure reduction and quality of life improvements in people with epilepsy. Epilepsia 2002; 43: 535–8.[CrossRef][ISI][Medline]
Bohannon RW, Smith MB. Interrater reliability of a Modified Ashworth Scale of muscle spasticity. Phys Ther 1987; 67: 206–7.
Carlsson M, Hagberg G, Olsson I. Clinical and aetiological aspects of epilepsy in children with cerebral palsy. Dev Med Child Neurol 2003; 45: 371–6.[CrossRef][ISI][Medline]
Chassoux F, Devaux B, Landré E, Chodkiewicz JP, Talairach J. Chauvel P. Postoperative motor deficits and recovery after cortical resections. Adv Neurol 1999; 81: 189–99.[Medline]
Chen LS, Wang N, Lin M. Seizure outcome of intractable partial epilepsy in children. Ped Neurol 2002; 26: 282–7.[CrossRef][ISI][Medline]
Chen R, Cohen LG, Hallett M. Nervous system reorganization following injury. [Review]. Neuroscience 2002; 111: 761–73.[CrossRef][ISI][Medline]
Custers JWH. Pediatric Evaluation of Disability Inventory: the Dutch adaptation. PhD thesis, Utrecht University; 2001.
Custers JWH, van der Net J, Hoijtink H, Wassenberg-Severijnen JE, Vermeer A, Helders PJM. Discriminative validity of the Dutch Pediatric Evaluation of Disability Inventory. Arch Phys Med Rehabil 2002; 83: 1437–41.[CrossRef][ISI][Medline]
Devlin AM, Cross JH, Harkness W, Chong WK, Harding B, Vargha-Khadem F, et al. Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence. Brain 2003; 126: 556–66.
Empelen R van, Jennekens-Schinkel A, Buskens E, Helders PJM, Nieuwenhuizen O van. Functional consequences of hemispherectomy. Brain 2004; 127: 2071–9.
Engel JJ, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel JJ, editor. Surgical treatment of the epilepsies. 2nd ed. New York: Raven Press; 1993. p. 609–21.
Feldman AB, Haley SM, Coryell J. Concurrent and construct validity of the Pediatric Evaluation of Disability Inventory. Phys Ther 1990; 70: 602–10.
Gorter JW, Rosenbaum PL, Hanna SE, Palisano RJ, Bartlett DJ, Russell DJ, et al. Limb distribution, motor impairment, and functional classification of cerebral palsy. Dev Med Child Neurol 2004; 46: 461–7.[CrossRef][ISI][Medline]
Graveline C, Hwang P, Bone G, Shikolka C, Wade S, Crawley A, et al. Evaluation of gross and fine motor functions in children with hemidecortication: predictors of outcomes and timing of surgery. J Child Neurol 1999; 14: 304–15.
Graveline C, Young N, Hwang P. Disability evaluation in children with hemidecorticectomy: use of the activity scales for kids and the pediatric evaluation disability inventory. J Child Neurol 2000; 15: 7–14.
Haley SM, Coster WJ, Ludlow LH. Pediatric Evaluation of Disability Inventory (PEDI) [manual]. Boston (MA): New England Medical Center; 1992.
Henderson SE, Sugden DA. Movement Assessment Battery for Children [manual]. London: Psychological Corporation; 1992.
Hislop HJ, Montgomery J. Daniels and Worthingham's Muscle testing techniques of manual examination. Philadelphia: W. B. Saunders; 2002.
Iyer LV, Haley SM, Watkins MP, Dumas HM. Establishing minimal clinically important differences for scores on the Pediatric Evaluation of Disability Inventory for inpatient rehabilitation. Phys Ther 2003; 83: 888–98.
Ketelaar M, Vermeer A, Hart H, van Petegem-van Beek E, Helders PJM. Effects of a functional therapy program on motor abilities of children with cerebral palsy. Phys Ther 2001; 81: 1534–45.
Krsek P, Tichy M, Belsan T, Zamecnik J, Paulas L, Faladova L, et al. Life-saving epilepsy surgery for status epilepticus caused by cortical dysplasia. Epileptic Disord 2002; 4: 203–8.[ISI][Medline]
Lendt M, Helmstaedter C, Kuczaty S, Schramm J, Elger CE. Behavioural disorders in children with epilepsy: Early improvement after surgery. J Neurol Neurosurg and Psychiatry 2000; 69: 739–44.
Medical Research Council. Aids to the investigation of peripheral nerve injuries. War memorandum 2nd ed. London: HMSO; 1943.
Nichols DS, Case-Smith J. Reliability and validity of the Pediatric Evaluation of Disability Inventory. Ped Phys Ther 1996; 8: 15–24.
Østensjo S, Carlberg EB, Vollestad NK. Motor impairments in young children with cerebral palsy: relationship to gross motor function and everyday activities. Dev Med Child Neurol 2004; 46: 580–9.[CrossRef][ISI][Medline]
Palisano RJ, Rosenbaum PL, Walter SD, Russell DJ, Wood EP, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997; 39: 214–23.[ISI][Medline]
Palisano RJ, Hanna SE, Rosenbaum PL, Russell DJ, Walter SD, Wood EP, et al. Validation of a model of gross motor function for children with cerebral palsy. Phys Ther 2000; 80: 974–85.
Peacock WJ, Comair Y, Hoffman HJ, Montes JL, Morrison G. Special considerations for epilepsy surgery in childhood. In: Engel JJ, ed. Surgical Treatment of the Epilepsies. 2nd edn. New York: Raven Press; 1993. p. 541–7.
Romanelli P, Weiner HL, Najjar S, Devinsky O. Bilateral resective epilepsy surgery in a child with tuberous sclerosis: case report. Neurosurg 2001; 49: 732–5.
Ronen GM, Streiner DL, Rosenbaum P; Canadian Pediatric Epilepsy Network. Health-related quality of life in children with epilepsy: development and validation of self-report and parent proxy measures. Epilepsia 2003a; 44: 598–612.[CrossRef][ISI][Medline]
Ronen GM, Streiner DL, Rosenbaum P. Health-related quality of life in childhood epilepsy: Moving beyond ‘seizure control with minimal adverse effects’. Health Qual Life Outcomes 2003b; 1: 36.[CrossRef][Medline]
Rosenbaum PL, Walter SD, Hanna SE, Palisano RJ, Russell DJ, Raina P, et al. Prognosis for gross motor function in cerebral palsy: creation of motor development curves. JAMA 2002; 18: 1357–63.
Russell D, Rosenbaum PL, Gowland C, Hardy S, Lane M, Plews N, et al. Manual for the Gross Motor Function Measure. 2nd edn. Hamilton (Canada): McMaster University; 1993.
Russell DJ, Rosenbaum PL, Avery LM, Lane M. GMFM Gross Motor Function Measure (GMFM-66 and GMFM-88) user's manual. Cambridge: Cambridge University Press; 2002.
Smith ML, Elliott IM, Lach L. Cognitive, psychosocial, and family function one year after pediatric epilepsy surgery. Epilepsia 2004; 45: 650–60.[CrossRef][ISI][Medline]
Smits-Engelsman BCM. Movement ABC. Nederlandse handleiding [manual]. Lisse: Swets & Zeitlinger; 1998.
Spiegel TM, Spiegel JS, Paulus HE. The Joint Alignment and Motion Scale; a simple measure of joint deformity in patients with rheumatoid arthritis. J Rheumatol 1987; 14: 887–93.[ISI][Medline]
Wood EP, Rosenbaum PL. The Gross Motor Function Classification System for cerebral palsy. Dev Med Child Neurol 2000; 42: 292–6.[CrossRef][ISI][Medline]
Wyllie E, Comair YG, Kotagal P, Bulacio J, Bingaman W, Ruggieri P. Seizure outcome after epilepsy surgery in children and adolescents. Ann Neurol 1998; 44: 740–8.[CrossRef][ISI][Medline]
World Health Organization. International Classification of Functioning, Disability and Health. Geneva: WHO; 2001.
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