Epilepsy & Behavior 67 (2017) 111–121

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Epilepsy & Behavior

journal homepage: www.elsevier.com/locate/yebeh

Neurorehabilitation with FORAMENRehab for attention impairment in

children with epilepsy
Marianne Saard a,b,⁎, Mari-Liis Kaldoja c,d, Madis Bachmann e, Lisanna Pertens e, Anneli Kolk a,b
a
Department of Pediatrics, Faculty of Medicine, University of Tartu, Tartu, Estonia
b
Department of Neurology and Neurorehabilitation, Children's Clinic, Tartu University Hospital, Tartu, Estonia
c
School of Educational Sciences, Tallinn University, Tallinn, Estonia
d
Department of Neurology and Rehabilitation, Tallinn Children's Hospital, Tallinn, Estonia
e
Institute of Psychology, University of Tartu, Tartu, Estonia

a r t i c l e i n f o a b s t r a c t

Article history: Epilepsy is a frequent neurological disorder in children and often accompanied with attention impairment. Still,
Received 22 March 2016 few systematically controlled rehabilitation techniques for children exist. The aim of this study was to design and
Revised 15 December 2016 measure the impact of the FORAMENRehab computer-based intervention method for attention impairment
Accepted 17 December 2016
rehabilitation in children with epilepsy. We chose the FORAMENRehab program because it allows separate train-
Available online xxxx
ing for different attention components based on individual needs.
Keywords:
Forty-eight children participated in the study. At baseline, all patients underwent neuropsychological examina-
Epilepsy tion of attention with the NEPSY test battery. The study group consisted of 17 8- to 12-year-old children with par-
Attention impairment tial epilepsy and attention impairment who received neurorehabilitation over 5 weeks (10 sessions) with
Cognitive rehabilitation FORAMENRehab Attention module accompanied by a therapist. Two control groups were included: the first con-
Computer-based neurorehabilitation in trol group of 12 children with partial epilepsy and attention impairment (waiting-list) participated in assessments
children with baseline tasks before and after the five-week period and received no active training. Additionally, all patients
FORAMENRehab program participated in the follow-up assessment 1.31 years later. The second control group consisted of 19 typically devel-
oping children who only participated in the first assessment.
After the intervention, study group patients showed significant improvement in complex attention and tracking
(P b 0.025). To achieve the effect of intervention in children with partial epilepsy, 10 sessions tailored to individ-
ual levels of ability were the minimum. Three attention components – sustained, complex, and tracking – need
selective and longer training for more effective remediation. Follow-up assessment revealed a long-term positive
effect of intervention. After 1.31 years, the study group had significantly improved in three out of the four
attention components (P b 0.025), whereas the waiting-list group showed improvement in only two aspects of
one complex attention component. In conclusion, attention impairment rehabilitation with FORAMENRehab is
effective for children with epilepsy. Rehabilitation should focus on training specific components of attention
and follow an individual-based rehabilitation process.
© 2016 Elsevier Inc. All rights reserved.

1. Introduction learning, memory, communication, problem solving, and perception

[2]. Sohlberg and Mateer [3,4] have differentiated at least four categories
1.1. Attention of models for attention: clinical models, factor analytic models,
cognitive processing models, and neuroanatomic models. The current
As one of the key components of cognitive functioning, attention has study is based on a clinical model of attention by Sohlberg and Mateer
been described as the processes that enable a person to concentrate on [2,3,5], in which attention consists of five interrelated components:
specific cognitive tasks and ignore others [1]. Attention is a multidimen- focused, sustained, selective, alternating, and divided attention. Focus-
sional cognitive process that affects other dimensions of cognition – ing and sustaining attention are considered lower-level processes,
whereas selective, alternating, and divided attention are more complex
processes that at least partially rely on the proper working of lower-
⁎ Corresponding author at: Department of Paediatrics, Faculty of Medicine, University of
level processes [2,3,5]. Tracking is also seen as part of complex attention
Tartu, N. Lunini 6, EE-51014 Tartu, Estonia. and is especially crucial when attention is needed while doing some
E-mail address: mariannesaard@gmail.com (M. Saard). other mental task (e.g., digit span backwards in a task concept) [6].

http://dx.doi.org/10.1016/j.yebeh.2016.12.030
1525-5050/© 2016 Elsevier Inc. All rights reserved.
112 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121

1.2. Attention impairment in pediatric epilepsy While the results of the FORAMENRehab pilot study were promising,
the need for modifications to improve the overall outcome of attention
Impairments of attention accompany various disorders including rehabilitation became apparent, as was more thoroughly described in
epilepsy [7], which is one of the most common neurological disorders the previous study [33]. In the current study a larger sample size, a
in children and adolescents. Children with different types of epilepsy waiting-list control group, and follow-up assessments were included.
and epilepsy syndromes have clearly expressed dysfunctions in differ- The main aim of the current research was to test the effectiveness of
ent attention components. Impairments in overall attention [8–11], a computer-based rehabilitation method with the Attention module of
sustained attention [12–14], selective attention [9], and alertness [15] the FORAMENRehab program in attention impairment rehabilitation
have been described. Both modalities, visual and auditory attention, for children with epilepsy aged 8–12 years.
have been found to be affected [16–18]. Furthermore, a recent study The specific aims were:
by Rathouz et al. [10] claims that cognitive deficits in children with
epilepsy that are present at baseline assessment are maintained for up 1. to examine the rehabilitation effect on specific attention components
to at least 5–6 years. This constitutes a prevalent problem in 8- to 12-year-old children using the FORAMENRehab program;
in the educational quality of these children. More so, attention impair- 2. to discover the optimal difficulty levels and duration of training for
ment is closely linked to impairments in other cognitive functions attention impairment;
(e.g., working memory and executive functions) [19]. As attention 3. to measure the long-term rehabilitation effect in follow-up
is crucial for learning, impairments in attention have been found to assessments;
contribute as a major negative influence on academic and social compe- 4. to evaluate the generalized effect and provide clinical implications
tences [20,21]. for computer-based attention rehabilitation in children with partial
epilepsy.

1.3. Attention rehabilitation in children

2. Methods
One suitable intervention method to facilitate cognitive perfor-
2.1. Participants
mance is cognitive rehabilitation (CR), which focuses on improving
a person's functioning in their everyday life by increasing their ability
2.1.1. Study group
to do what they need and like, but find difficult or impossible due to
The current study was carried out from May 2012 until March 2015
their cognitive disability [22,23]. Cicerone et al. [24] concludes that in
in the Department of Neurology and Neurorehabilitation at the
order to contribute to the generalization effect, the training should be
Children's Clinic of Tartu University Hospital. The study was approved
addressed to specific attention functions and teaching strategies.
by the Research Ethics Committee of the University of Tartu.
Cognitive rehabilitation in children with attention impairments is
In the intervention, 17 children aged 8–12 years with attention
nowadays mainly developed into computer-based interventions. Chil-
impairment and diagnosis of partial epilepsy participated. There
dren surviving cerebral malaria [25,26], children with HIV [27], and sur-
were 12 boys and 5 girls in the intervention group (see Table 2 for
vivors of childhood cancer [28] have been trained with Captain's Log
further details). The age group was chosen based on methodological
cognitive training software with immediate benefit to attention skills.
considerations: 1) the children were required to have sufficient reading
Lee et al. [29] and Galbiati et al. [30], who trained children with traumat-
and basic mathematical skills; 2) to keep the age range and develop-
ic brain injury, found that attention-specific neuropsychological train-
mental level of the children comparable.
ing significantly improved attention performance.
Participants were chosen according to the following inclusion
As for epilepsy, very few studies have investigated the effects of cog-
criteria:
nitive rehabilitation programs for attention impairments. The amount
of research is still modest compared to other acquired brain injury diag-
noses and has mostly been conducted on adult patients with epilepsy. 1. Previously diagnosed partial epilepsy (ICD-10 G40.0, G40.1, G40.2);
Engelberts et al. [31] used two training methods for attention rehabilita- diagnosis confirmed by a child neurologist.
tion on adults with focal seizures – the Retraining Method and the 2. Mild to moderate attention impairment stated by parents and
Compensation Method – and found both to be effective in improving teachers and confirmed by a certified clinical neuropsychologist on
the patients' cognitive outcomes. Gupta and Naorem [32] stated that the basis of neuropsychological assessment. The assessment includ-
after specific cognitive training (including for attention deficits), using ed attention subtests from the NEPSY test battery (Tower Test, Visual
both paper and pencil tasks and real-life activities for patients with Attention, Auditory Attention and Response Set, Statue, Design
epilepsy, overall improvement in cognitive performance occurred. Fluency, Knock and Tap). Minimum and maximum scores of patients
However, for children with epilepsy, very few modern neurocognitive for each subtest are included in Table 1.
rehabilitation techniques exist, and most of the available methods 3. Fluency in Estonian (first spoken language);
used are designed for adults. A positive outcome in remediation of 4. Age between 8 and 12 years;
attention impairment in children with epilepsy was revealed with our 5. Parental written consent and child's verbal agreement to participate
pilot study using the FORAMENRehab computer-program. After a six- in the intervention.
week, therapist-guided, and personalized training program, sustained
attention and complex attention of children showed significant
improvements. No significant changes were detected in focused Table 1
attention and tracking. That said, parents and teachers of the Standardized score ranges for NEPSY subtests; normal range 7–13.
participating patients also stated positive changes in behavior and an
NEPSY subtest Min score Max score
increase in academic achievement, suggesting a generalized effect of 29 patients
the intervention [33].
Tower 1 14
There is therefore an unmet need for more accurate and Visual attention 2 19
systematically controlled research in pediatric cognitive rehabilitation Auditory attention 3 15
[34–36]. More so, the field of neuropsychological rehabilitation needs Statue 1 12
guidelines and underlying principles in order to inform the work Design fluency 2 18
Knock and tap 2 13
of clinicians [37,38].
 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121 113

Exclusion criteria included other documented diseases involving The exercises are playful and last from 1 to 4 min (with the excep-
the central nervous system (e.g., stroke, tumors, encephalitis, cerebral tion of a sustained attention task which can take up to 20 min). The
palsy), psychiatric co-morbidity (e.g., ADHD, anxiety disorder, mental menu structure, toolbar, and icons of the software are illustrative;
retardation (ICD-10 F70-F79)), and treatment with any psychotropic each task has clear written instructions as well as a model animation.
medication other than antiepileptic drugs during the rehabilitation The parameters of each task are adjustable. The results are given both
period. In summary, the sample of children with epilepsy included 4 in numerical tables and graphs. Several outcomes are recorded for
newly-diagnosed patients, the maximum duration of epilepsy for a every application: solving and/or reaction time, number of correct re-
single child was 5.08 years, and 1 patient was on polytherapy, while sponses, and subcategories of mistakes (omission errors, premature re-
16 were on monotherapy. All 17 children attended all 10 training sponses, commission errors, and total number of errors – sum of
sessions – therefore, compliance with the intervention was 100%. omission and commission errors).

2.1.2. Control groups 2.3. Rehabilitation procedure

Two control groups were included in the study – waiting-list control
group and healthy children's control group. The rehabilitation of patients took place during 6 weeks with a
5-week training period. Thirteen meetings were conducted with each
1. The waiting-list control group was composed of 12 children with patient: the first baseline assessment, altogether 10 active training ses-
epilepsy aged 8–12 years with attention impairment who could not sions with meetings twice a week, and the second assessment with
participate in the intervention. There were 9 boys and 3 girls in the baseline tasks (primary outcome). Also, the final follow-up assessment
group (see Table 2 for further details). The inclusion and exclusion with baseline tasks as the secondary outcome was conducted 1.31 years
criteria were the same as for the intervention group. The study (SD = 0.40) after the training period (third assessment with baseline
group and waiting-list group did not differ significantly regarding tasks). In total, 10 children from the study group and 9 children from
the age at epilepsy onset. Children with epilepsy who participated the waiting-list group participated in the final follow-up.
either in the study or waiting-list group were diagnosed with partial Training sessions occurred in an outpatient setting in the Children's
epilepsy and the seizures were well-controlled by medication. Also, Clinic. The time for each individual session varied between 30 and
the children all attended regular schools and did not receive special 40 min.
education. Additionally, all patients were presented at first with an At the first meeting the intervention methods and goals were intro-
opportunity to participate in the rehabilitation. Frequently, children duced to the patient. Thereafter, the first performance of baseline tasks
from outside the Tartu city boundary could not regularly attend the was conducted to assess the child's initial profile of attention compo-
intervention due to difficulties with transportation and were there- nents. The training sessions started at the second meeting.
fore assigned to the waiting-list group. Each meeting was conducted by one of the four therapists, who
were all psychologists working in the hospital. The therapists received
2. To assess the baseline levels for attention tasks and to obtain results training before administering the rehabilitation and followed a stan-
representing the healthy population, the healthy children's control dardized protocol. Throughout, the therapists did not only introduce
group was composed of 19 healthy age-matched children aged the tasks, but also motivated and guided the child individually in
8–12 years. There were 11 boys and 8 girls in the control group. order to help him/her to cope better with new and complicated situa-
The children were recruited from an ordinary school in Tartu and tions and to apply the learned techniques to everyday life. Furthermore,
attended 2nd to 5th grades. Parental written consent and the child's an important part of the training process is the therapist-guided
verbal consent to participate in the study were received. Children metacognitive study experience for children, which teaches different
with any known neurologic or psychiatric diagnosis were excluded learning and problem-solving strategies.
from the control group. The study group and two control groups A strict protocol for our intervention procedure was created. For
did not differ significantly in terms of age and sex. assessing the effectiveness of the rehabilitation, the baseline tasks
were tested once more at the last meeting of the six-week period and
also finally 1.31 (SD = 0.40) years later to measure sustained long-
2.2. Rehabilitation software
term effects. The generalized effect of the APT was evaluated by parent
and child questionnaires about the perceived attention, behavior, and
The FORAMENRehab Cognitive Rehabilitation Software®
school performance, in addition to objective baseline assessments.
(FORAMENRehab) was used in the study. FORAMENRehab is a tool
For this purpose we developed a Likert-type scale, which was used to
for cognitive rehabilitation that was developed in 2000 by Koskinen
compare periods before and after the intervention.
and Sarajuuri [39] in Finland. It was adapted for Estonian children in
our pilot study [33]. Due to the variability of the tasks, the software
can be used for children with acquired or developmental disorders. In 2.4. Rehabilitation designs for FORAMENRehab software
the present study, the Attention module was implemented. Different
components of attention function were assessed and trained with the Two different intervention designs were used in the process of
module. The tasks were divided into four categories or components – fo- conducting the intervention and evaluating the appropriateness of the
cused attention, sustained attention, complex attention, and tracking. FORAMENRehab computer program. First, a pilot study was conducted

Table 2
Study group and waiting-list control group characteristics.

Group Nr of patients Age at intervention (yrs) Age at epilepsy onset (yrs) Duration of epilepsy (yrs)
(M/F) Mean (95%CI)a Mean (95%CI) Mean (95%CI)

Study n = 17 (12/5) 9.95 (9.33…10.57) 7.85 (6.92…8.78) 2.10 (1.34…2.86)

Waiting-list n = 12 (9/3) 10.20 (9.08…11.32) 8.27 (7.22…9.32) 1.97 (0.60…3.33)
Sig. P⁎ 0.9647 0.3637 0.3512

M – male, F – female, yrs – years.

a
Mean score (95% confidence intervals for Mean).
⁎ Cut-off P value for significance is 0.05.
114 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121

Meeting no. 1 2 3 4 5 6 7 8 9 10 11 12 13 Follow-up

Interventional trainings
Baseline Baseline ass Baseline
1.31yrs
assessment 1 5 weeks ssment 2 assessment 3
1 2 3 4 5 6 7 8 9 10

Fig. 1. Design of the intervention.

[33], and based on the results the intervention protocol was modified to outcome assessment, and follow-up or secondary outcome assessment.
better differentiate children's baseline impairment profiles, to more During the five-week period between the first and the second assess-
accurately measure the rehabilitation effect, and to facilitate progress ment, the waiting-list group received no intervention. One-time testing
at each difficulty level during training. The new procedure protocol of healthy control children took place in their school setting.
for the intervention that was created is shown in Fig. 1. The results re-
ported in this paper are based on the new design. 2.6. Data analysis
In the baseline assessment, all four components of attention were
tested. Two to three tasks from each component were chosen. For train- Statistical data analysis was performed with the R version 3.1.2. For
ing sessions, other tasks involving the same attention components were some of the figures, the SAS data analysis package 9.2 was used. The
used, divided into three difficulty levels: easy (I), medium (II), and dif- Kolmogorov-Smirnov test was used for the assessment of normality.
ficult (III) (see Table 3 for detailed description). Some tasks were divid- Wilcoxon-Mann-Whitney test was used to compare the study group
ed into two difficulty levels as there were either no easy or difficult and controls on each of the attention variables. For each task, different
settings for children. components of performance were evaluated if possible (correct
Development at each difficulty level was individual-based and responses, omission and commission errors, total number of mistakes,
depended on the child's personal improvement. If the child was flawless reaction time, and processing speed).
at the task, he/she advanced to the next level of the same attention com- We used linear mixed models to assess whether longitudinal
ponent at the next training session. If the child's response was incorrect, changes in groups were overall significantly different. We com-
he/she had to perform the same task level at least 80–90% correctly pared the baseline performance to primary (immediate interven-
(depending on the task) for 3 meetings consecutively until advancing tion effect) and secondary outcomes within the study group and
to the next difficulty level. This affirmed that the child had acquired waiting-list control group. For comparing proportions (qualitative
the requested abilities. variables) the McNemar's test was used. The confidence level was
set to 5%. We controlled the false discovery rate (FDR) to be lower
2.5. Testing of the controls than 5% by using linear step-up procedure (Benjamini and
Hochberg 1995) [40] for multiple t-tests. Benjamini-Hochberg crit-
The children in the waiting-list control group participated in ical values were calculated as (i/m)Q, where i is the rank in an as-
three assessments with baseline tasks – the first assessment, primary cending list of P values, m is the total number of tests, and Q is a

Table 3
Difficulty levels in tasks under four attention components and the affected attention functions.

Easy Medium Difficult Affected attention functions

Focused attention
Visual reaction time Visual reaction time; auditory warning Visual multiple choice Attention activation, alertness and selectivity:
visual choice reaction time reaction time simple visual or auditory reaction (intrinsic
Auditory reaction time Auditory reaction time; visual warning Auditory multiple choice vigilance); tasks with warning (phasic activation of
auditory choice reaction time reaction time attention) or with distracting stimuli (selective
attention and reaction inhibition).

Sustained attention
Single figure search with letter, number, (Medium level) (Difficult level) Continuous attention, finding high ratio of relevant
symbol I, symbol II, or picture (easy level) stimuli, processing speed, correctness
Series search with letter, number, figure, or (Medium level) (Difficult level)
symbol series (easy level)
Paced search with single target (Target length – 4 characters; (Target length – 7 characters)
(target length – 2 characters) target shifting interval – faster)
– Repeated pairs search with symbols Repeated pairs search Continuous attention, high ratio of disturbing
with letters stimuli.

Complex attention
Paced search with dual targets (Target length – 3 characters; faster (Faster stimulus interval – Dual tasks: dividing and shifting attention,
(target length – 2 characters; speed – 1,5 s; stimulus interval – speed – 1 s) speed 0.7 s) cognitive flexibility.
direction – right)
Addition; single number (Series length – 6–8 digits; faster Addition; dual numbers Single addition: dividing attention, working
(series length – 4 digits; speed – 1.5 s) stimulus interval) memory.
Word recognition; single target Word recognition; dual targets Simultaneous word Single word recognition: continuous attention,
recognition and mental comparison with existing knowledge.
arithmetic

Tracking
Tracking task Continuous attention, attention activation.
PASAT; visual presentation PASAT; visual presentation – Visual dividing of attention, executive function of
(faster stimulus interval) working memory.

PASAT - Paced Auditory Serial Addition Test.

 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121 115

Table 4
Comparison of performances on first baseline assessment between patients and healthy control children.

Parameters of FORAMENRehab Attention tasks Patients Controls db Sig. P

First baseline assessment (B1) Median (lower and upper quartiles)a Median (lower and upper quartiles)

Focused attention
Visual reaction time (s) 0.59 (0.49…0.67) 0.53 (0.43…0.65) 0.29 0.082
Auditory reaction time (s) 0.61 (0.54…0.74) 0.62 (0.59…0.69) −0.08 0.626

Sustained attention
Correct responses in picture search (%) 97.44 (94.87…98.72) 98.72 (96.15…100.00) −0.32 0.040⁎
Omission errors in picture searchc (%) 2.56 (0.00…3.85) 1.28 (0.00…3.85) 0.24 0.178
Processing speed in picture search (s) 205.00 (160.50…244.00) 159.00 (140.00…215.00) 0.38 0.026⁎
Processing speed in numbers search (s) 709.00 (597.00…886.00) 603.00 (393.00…747.00) 0.36 0.042⁎

Complex attention
Omission errors in paced search (%) 68.20 (53.94…83.85) 44.12 (25.81…61.11) 0.57 b0.001⁎
Total errors in paced searchd (nr) 32.00 (26.00…35.00) 22.00 (12.00…27.00) 0.58 b0.001⁎
Omission errors in word recognition (%) 58.33 (33.33…75.00) 19.87 (9.09…50.00) 0.66 0.0001⁎
Commission errors in word recognitione* (nr) 1.00 (1.00…2.00) 2.00 (1.00…3.00) −0.16 0.335
Correct responses in addition (%) 30.00 (15.00…65.00) 80.00 (70.00…90.00) −0.77 b0.0001⁎

Tracking
Correct responses in PASAT (%) 22.50 (10.00…30.00) 65.00 (45.00…95.00) −0.82 b0.0001⁎
Omission errors in PASAT (%) 50.00 (27.50…65.00) 17.50 (5.00…20.00) 0.63 0.0003⁎
Commission errors in PASAT (%) 22.50 (15.00…47.50) 12.50 (0.00…30.00) 0.43 0.013⁎
Commission errors in tracking task (nr) 1.0 (0.00…2.00) 0.00 (0.00…0.00) 0.40 0.013⁎
a
Median (lower 25%ile and upper 75%ile).
b
Effect size index Cliff's delta.
c
Omission errors – missed responses to target stimuli.
d
Total errors – sum of omission and commission errors.
e
Commission errors – responses to nontarget stimuli.
⁎ Cut-off P value for significance is 0.05.

false discovery rate of 0.05. The cut-off P value for significance in a 3. Results
single comparison for the longitudinal changes of attention vari-
ables in study group is 0.025. Only P values that are below the ad- 3.1. Differences in attention components in children with epilepsy and
justed FDR significance threshold are therefore significant and healthy controls
marked as such (*) in the tables. Effect sizes for non-normal distri-
butions were calculated using the Cliff's Delta statistic, which is a Comparison of performances on the FORAMENRehab baseline assess-
non-parametric effect size measure that quantifies the amount of dif- ment between children with epilepsy (including both the study group
ference between two groups of observations [41]. and waiting-list control group) and healthy children was conducted

Table 5
Primary outcome of attention function training in study group.

Parameters of FORAMENRehab Attention tasks Baseline B1 Primary outcome B2 Secondary outcome B3 B1-B2-B3 B1 vs B2 B1 vs B3
Study group (n = 17) Mean (95%CI)a Mean (95%CI) Mean (95%CI) Sig Pf Sig P Sig P

Focused attention
Visual reaction time (s) 0.64 (0.57…0.71) 0.67 (0.58…0.76) 0.51 (0.43…0.60) 0.0071 0.5715 0.0047⁎
Auditory reaction time (s) 0.66 (0.59…0.73) 0.67 (0.58…0.75) 0.58 (0.50…0.65) 0.1297 0.9115 0.0869

Sustained attention
Correct responses in picture search (%) 96.15 (93.59…100.00)e 98.72 (96.15…100.00)e 99.36 (97.44…100.00)e 0.1530 0.1864 0.0930
Omission errors in picture searchb (%) 3.85 (0.00… 6.41)e 1.28 (0.00…3.85)e 0.64 (0.00…2.56)e 0.1578 0.1922 0.0966
Processing speed in picture search (s) 185.71 (165.54…205.87) 210.94 (161.77…260.12) 182.10 (148.09…216.11) 0.4384 0.2927 0.2160
Processing speed in numbers search (s) 738.94 (588.32…889.56) 854.65 (675.19…1034.10) 575.00 (459.70…690.30) 0.0770 0.2783 0.1677

Complex attention
Omission errors in paced search (%) 66.74 (57.79…75.68) 41.99 (30.96…53.03) 33.94 (26.56…41.31) b0.0001 b0.0001⁎ b0.0001⁎
Total errors in paced searchc (nr) 32.19 (27.37…37.00) 18.35 (13.51…23.20) 17.67 (13.60…21.73) b0.0001 0.0002⁎ b0.0001⁎
Omission errors in word recognition (%) 56.15 (41.70…70.60) 38.78 (25.59…51.97) 20.76 (5.27…36.26) 0.0003 0.0028⁎ 0.0002⁎
Commission errors in word recognitiond (nr) 2.00 (1.00…2.00)e 1.00 (0.00…2.00)e 0.00 (0.00…2.00)e 0.1081 0.0744 0.0741
Correct responses in addition (%) 41.76 (26.75…56.78) 63.53 (49.57…77.49) 80.00 (68.82…91.18) 0.0002 0.0007⁎ 0.0002⁎

Tracking
Correct responses in PASAT (%) 25.88 (17.79…33.97) 55.29 (38.70…71.89) 67.00 (49.71…84.29) 0.0001 0.0002⁎ 0.0002⁎
Omission errors in PASAT (%) 36.80 (23.97…49.62) 29.70 (15.70…43.71) 17.00 (5.66…28.34) 0.1877 0.3600 0.0710
Commission errors in PASAT (%) 34.12 (20.51…47.73) 15.00 (8.08…21.92) 16.00 (4.71…27.29) 0.0164 0.0049⁎ 0.0475
Commission errors in tracking task (nr) 1.00 (0.00…1.50)e 1.00 (1.00…2.00)e 0.50 (0.00…1.00)e 0.4045 0.2526 0.2624
a
Mean score (95% confidence intervals for Mean).
b
Omission errors – missed responses to target stimuli.
c
Total errors – omission and commission errors.
d
Commission errors – responses to nontarget stimuli.
e
Median score (lower 25%ile and upper 75%ile), non-normal distribution.
f
Mixed models method.
⁎ Cut-off P value for significance in single comparison for longitudinal changes of attention variables is 0.023.
116 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121

Fig. 2. Means with 95% confidence interval for percent of correct responses in three complex attention tasks at three assessment points (B1-baseline, B2-primary outcome, B3-secondary
outcome) in study and control groups.

(see Table 4). In focused attention, the trend showed a quicker reaction of the measured attention components. But immediately after the inter-
time to visual stimuli in healthy children. In sustained attention, the chil- vention, noticeable improvements were seen in the study group as they
dren with epilepsy had a significantly worse overall performance com- had significantly improved complex attention and tracking components
pared to their healthy peers, as they demonstrated slower processing compared to the first baseline performance (for further details see
speed as well as a lower percentage of correct responses. In complex Table 5).
attention, the patients performed significantly worse than healthy After training, the study group patients performed significantly bet-
children in each aspect of the task: they gave significantly less correct ter in Paced Search with Dual Targets (complex attention): they gave
responses as they had more omission errors and total errors (sum of more correct responses, and had less omission errors and less total er-
omission and commission errors). In tracking, the patient group had sig- rors compared to the first assessment. In Word Recognition with Dual
nificantly worse results in every aspect compared to healthy controls. Targets (complex attention), the study patients had significantly more
correct responses and less omission errors. In this task, most of the
3.2. Primary outcome in two epilepsy groups before and after the children with epilepsy had some commission errors in baseline as
intervention period well as in primary outcome assessment. Thus, for more targeted exam-
ination we divided the groups into two by number of commission er-
3.2.1. Immediate rehabilitation effect (primary outcome) on specific rors, based on a cut-off point of 6 errors. A McNemar's test showed
components of attention in study group significant overall improvement: 86.7% of children belonged to the
At first there were no significant differences in performances at group with a greater number of mistakes at baseline assessment, but
baseline levels between study and waiting-list control groups in any only 26.67% at primary outcome assessment (P b 0.05). In Addition

Fig. 3. Means with 95% confidence interval for percent of correct responses, and commission and omission errors in PASAT under tracking component at three assessment points (B1-
baseline, B2-primary outcome, B3-secondary outcome) in study and control groups.
 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121 117

Fig. 4. Means with 95% confidence interval for visual and auditory reaction times in focused attention at three assessment points (B1-baseline, B2-primary outcome, B3-secondary
outcome) in study and control groups.

task (complex attention), the intervention group gave significantly 3.2.2. Second assessment or primary outcome with baseline tasks in the
more correct responses after rehabilitation (see Table 5). Fig. 2 shows waiting-list control group
the percentage of correct responses in the baseline, primary, and sec- After the 5-week period without intervention, the waiting-list
ondary outcome assessments. control group did not show any significant differences between the
Also, the study group patients had improved significantly after first and second assessment (see Table 6).
training in PASAT (tracking component): they gave more correct re- Different results for study and waiting-list control groups are
sponses and had less commissions. Fig. 3 shows the percentage of visually shown in Figs. 2–4.
correct responses for each aspect of PASAT in three assessment
points. 3.2.3. Comparison of second assessment with baseline tasks between study
No statistically significant dynamic changes were revealed in and waiting-list control groups
focused attention for reaction times (Fig. 4) or in sustained attention After the intervention, differences between performances in base-
for processing speed. line tasks had emerged between the study and waiting-list control

Table 6
Primary outcome of attention function training in waiting-list group.

Parameters of FORAMENRehab Attention tasks Baseline B1 Primary outcome B2 Secondary outcome B3 B1-B2-B3 B1 vs B2 B1 vs B3
Waiting-list group (n = 12) Mean (95%CI)a Mean (95%CI) Mean (95%CI) Sig Pf Sig P Sig P

Focused attention
Visual reaction time (s) 0.56 (0.50…0.61) 0.60 (0.49…0.70) 0.60 (0.49…0.71) 0.7498 0.6795 0.5517
Auditory reaction time (s) 0.66 (0.55…0.77) 0.70 (0.60…0.79) 0.67 (0.54…0.81) 0.8988 0.6571 0.8576

Sustained attention
Correct responses in picture search (%) 97.44 (96.15…98.72)e 96.15 (96.15…98.72)e 98.72 (97.44…98.72)e 0.7771 0.6082 0.8191
Omission errors in picture searchb (%) 2.56 (1.28… 3.85)e 3.85 (1.28… 3.85)e 1.28 (1.28… 2.56)e 0.3968 0.7818 0.3690
Processing speed in picture search (s) 238.20 (200.69…275.72) 224.67 (177.42…271.91) 218.33 (152.26…284.41) 0.4888 0.4334 0.2547
Processing speed in numbers search (s) 711 (566…912)e 969 (469.5…1144.5)e 544 (506…1101)e 0.7667 0.6911 0.7021

Complex attention
Omission errors in paced search (%) 68.88 (57.92…79.84) 65.33 (55.57…75.10) 51.42 (32.60…70.25) 0.0309 0.3246 0.0094⁎
Total errors in paced searchc (nr) 32.60 (23.80…41.41) 30.58 (23.81…37.35) 25.56 (14.86…36.25) 0.1855 0.2024 0.0774
Omission errors in word recognition (%) 59.30 (46.75…71.84) 52.08 (33.12…71.04) 42.30 (23.00…61.60) 0.1506 0.3099 0.0562
Commission errors in word recognitiond (nr) 1.00 (1.00…2.00)e 1.00 (0.00…3.00)e 1.00 (1.00…2.00)e 0.3725 0.2075 0.2574
Correct responses in addition (%) 33.33 (18.44…48.23) 36.67 (22.50…50.83) 58.89 (36.33…81.45) 0.0097 0.4418 0.0031⁎

Tracking
Correct responses in PASAT (%) 19.00 (12.04…25.96) 31.67 (17.37…45.96) 45.00 (21.88…68.11) 0.0894 0.0777 0.0327
Omission errors in PASAT (%) 56.00 (44.91…67.09) 40.83 (20.89…60.78) 39.38 (19.59…59.16) 0.1638 0.0800 0.1686
Commission errors in PASAT (%) 25.00 (15.58…34.42) 32.50 (16.97…48.03) 15.63 (8.07…48.03) 0.0287 0.4165 0.1297
Commission errors in tracking task (nr) 1.00 (1.00…2.00)e 0.50 (0.00…3.00)e 1.00 (0.00…2.00)e 0.9119 0.8750 0.6724
a
Mean score (95% confidence intervals for mean).
b
Omission errors – missed responses to target stimuli.
c
Total errors – omission and commission errors.
d
Commission errors – responses to nontarget stimuli.
e
Median score (lower 25%ile and upper 75%ile), non-normal distribution.
f
Mixed models method.
⁎ Cut-off P value for significance in single comparison for longitudinal changes of attention variables is 0.023.
118 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121

Table 7
Average attained difficulty levels at the end of intervention in four attention components.

Attention component Nr of task Mean level 95% confidence interval

Focused attention 1 3.88 3.69 4.06

2 4 –
Sustained attention 1 3.31 2.94 3.69
2 3 2.81 3.19
3 3.56 3.23 3.9
Complex attention 1 1.19a 0.97 1.4
2 1.62a 1.3 1.95
3 1.88a 1.61 2.14
Tracking 1 1.31a 0.99 1.63
a
Tasks with slower progress.

groups. The second assessment showed that the study group had signif-
icantly better results in complex attention and tracking compared to the
waiting-list group. In Paced Search, they had a higher percentage of
correct responses (P b 0.01), less omission errors (P b 0.01), and less
total mistakes (P b 0.01). In Addition and PASAT tasks, they had a higher
percentage of correct responses (P b 0.05 and P b 0.05, respectively).
Trends also showed fewer mistakes in the Auditory Choice Reaction
Fig. 5. Children's individual progress trajectories for 10 training sessions (summary score
Time task (P = 0.089) and less commission errors in Picture Search in
per visit).
the study group (P = 0.061).

3.3. Patients' individual improvement during rehabilitation process errors, and lower percentage of total errors. In the tracking component,
they had significantly more correct responses and a trend toward less
We also examined the study group children's individual improve- commission errors.
ment during the rehabilitation process and advancement in reaching It is noteworthy that the waiting-list group performed significantly
higher difficulty levels. A slower rehabilitation effect out of the four better compared to baseline performance in only two aspects of complex
attention components occurred in two: complex attention and tracking - attention tasks (see details in Table 6).
where children's average attained level at the end of training was only Figs. 2–4 show long-term results for both groups and the compari-
1.55 (95% CI: 1.36…1.74) out of a maximum of 4 and 1.31 out of a son with primary and secondary outcomes in baseline tasks.
maximum of 3, respectively (see Table 7 for further details).
In order to assess the degree of difficulty of the tasks, the average
3.5. Generalized effect of attention rehabilitation
number of training sessions at the first difficulty level needed to prog-
ress to the second level was measured for each task (see Table 8).
All children and 9 parents gave feedback about the intervention
All children had positive individual progress throughout the inter-
effect. Subjective feedback from parents suggested positive behavioral
vention as they gradually reached higher difficulty levels. Still, the
change in children. As a manifestation of the generalized effect, the
speed of progress was different individually for each child. At the end
parents stated that their children were less distracted and more likely
of training, children with faster progress had attained approximately
to engage in social communication. Also, according to the parent re-
1.5–2 times higher difficulty levels compared to the children with
ports, reading, writing, mathematics, and visuomotor skills had im-
slower progress (see Fig. 5).
proved. Children stated improved concentration skills and better
functioning in school tasks.
3.4. Follow-up or secondary outcome

In the follow-up assessment 1.31 years later – the secondary 4. Discussion

outcome – the study group showed significant positive long-term
effects of intervention (see details in Table 5). In focused attention, the This research was conducted to test a modern computer-based in-
reaction time to visual stimuli was significantly faster compared to the tervention method for children with attention impairment and examine
first baseline performance. Also, improvements existed in all complex the rehabilitation effect on different attention components.
attention tasks: a higher percentage of correct responses, less omission
4.1. Effective computer-based rehabilitation method for children with an
individual-based intervention protocol
Table 8
Average number of trainings attended before moving from first difficulty level to second In order to specifically illustrate the attention impairment profiles of
level.
children with epilepsy, in addition to neuropsychological assessment,
Attention component Nr of task Mean sessions 95% confidence interval the baseline tasks of the FORAMENRehab Attention module were
1 1.75 1.22 2.28 used. Our results demonstrated that the assessment successfully differ-
Focused attention
2 1.56 1.01 2.11 entiated children with epilepsy from their healthy peers as their perfor-
1 2.12 1.51 2.74 mance levels were significantly lower in three out of the four measured
Sustained attention 2 1.38 0.99 1.76
attention components. Therefore, the baseline tasks demonstrated a
3 1.62 1.2 2.05
1 7.69a 6.56 8.82 significant need for further intervention for the children with epilepsy.
Complex attention 2 5.81a 4.46 7.16 The current study demonstrated that the Attention module of the
3 4.62a 3.37 5.88 computer-based intervention program FORAMENRehab is a suitable
Tracking 1 5.62a 4.69 6.56 method for children with epilepsy. The rehabilitation design success-
a
Tasks with slower progress. fully supported continuous progress during the intervention process
 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121 119

in different attention components. One of the strengths of this method processes of a task improved during training, and therefore the ability
is that it is tailored to follow each individual's abilities and attention to simultaneously process information received either a short time ear-
impairment profile. Amonn et al. [42] stated that in order to prove clin- lier or in the moment was positively affected.
ical value, cognitive training programs should “focus more strongly on In focused attention, no significant change was discovered when
individually existing neuropsychological deficits”. The training protocol measuring visual and auditory reaction times; similar results have
used in this study allowed the observation of progress in each individual been reported by Van't Hooft et al. [49] and Cicerone [51]. Just like
child as well as the children's overall progress within attention compo- Van't Hooft et al. [49], we also believe that although training might
nents, and enabled comparison of outcomes between children and not improve reaction times, it still provides the children with valuable
groups. solution techniques and strategies.
The rehabilitation of children is different from interventions for Furthermore, by measuring children's individual progress at each
adults because children do not enter the process through their own difficulty level, distinctive differences in the more complicated attention
initiative. Therefore, they need continuous guidance and motivation components were revealed. At the end of rehabilitation, the study group
throughout the rehabilitation period. According to Cicerone et al. [43], remained at lower difficulty levels in complex attention and tracking
active therapist involvement enhances the overall effectiveness of reha- components compared to focused and sustained attention. Although
bilitation. Our design involves a therapist to help make individual the comparison with baseline tasks showed significant improvements
plans by following each child's progress, and who follows the training in complex attention and tracking, these components would need lon-
protocol. The therapist motivates the child and supports the use of ger training for more effective remediation.
acquired skills in everyday life situations. Charvátová et al. [44] pointed The positive rehabilitation effect in the intervention group was
out that children do not make a strict distinction between games, work, further confirmed in comparison with the waiting-list group. After the
leisure, and educational activities, but the crucial characteristics are mo- 5-week period without intervention, the waiting-list group demon-
tivation, competitiveness, emotions, and natural curiosity. This con- strated no significant change between the first and second assessment
vinces us of the importance of a therapist in the rehabilitation process. with baseline tasks. Furthermore, the follow-up assessment after
Children with epilepsy have also previously shown improved behavior- 1.31 years showed the sustained, positive, long-term effect of rehabilita-
al performance when presented with rewards which could provide sig- tion in the study group, in contrast to the children in the waiting-list
nificant benefit in cognitive remediation programs [45]. Our study group who demonstrated remarkably less positive dynamics over time
implies that guided intervention is especially valuable in children with (aside from the developmental curve). This emphasizes the effective-
attention impairment, as they continually need extra help in directing ness of intervention and diminishes the chance of a positive outcome
attention to tasks. It leads the child to become more aware of different solely due to normal developmental processes. Thereafter, the parents
options and to learn to compensate for cognitive weaknesses. Therefore, conclusively confirmed the sustained positive effect and reported
it could help them to become more independent in the learning process. noticeable positive changes in their children's everyday life situations.
Our experience showed that if the child understands the solution pro- The generalized effect of rehabilitation manifested in the children's
cess by using a specific strategy, he/she has a successful experience behavior and overall performance in school.
and gains motivation and self-confidence. The children were more at- It was also valuable that the family became aware of the children's
tentive in classes and in solving homework – they improved in cognitive strengths and weaknesses as well as the importance of cogni-
pinpointing mistakes, revising work, finding solutions to problems, tive rehabilitation. In the end, full compliance and positive feedback
etc. Therefore, the support from the therapist might have also contribut- from children showed that the computer-based neurorehabilitation is
ed to the effect of the training. It is a valuable additional benefit to the pleasurable for children.
intervention; children with epilepsy have been reported to perceive
stigma associated with the “need for information and support” [46],
and present with emotional problems [47]. 4.3. Clinical implications for rehabilitation
The Neuropsychology Task Force of the International League Against
Epilepsy (ILAE) stated the importance of providing the patients' families Developing an intervention design with a specific protocol and well-
with implications of assessment results and clinical recommendations defined instructions for therapists is recommended. In a review by
regarding what can be done for cognitive improvement [48]. In our Sohlberg et al. [52] the importance of giving systematic instructions in
study, the parents received personal feedback about their child's atten- cognitive rehabilitation is emphasized. These should consist of “simple,
tion profile, progress throughout the training, and suggestions for future consistent instructional wording and scripts to reduce confusion and
training possibilities at home (e.g., via the Internet). They were also pro- focus the learner on relevant content”.
vided with additional advice for supporting their child's general learn- In addition, based on qualitative feedback, we noted that an
ing abilities and for considering their child's individual differences. important task for the therapist is to find specific motifs for each
individual child. (e.g., for the best cooperation some children pre-
4.2. Effects of rehabilitation in the study group ferred joking, some needed little breaks after a while, and others
hoped for frequent appraisal and endorsement). Yet some children
Effects of rehabilitation were studied by comparing the perfor- also required more specific boundaries to keep them on track. In
mances in baseline tasks (used only for examination) before and after some cases, children preferred the therapist to be of the same gender
the intervention period. After active training for five weeks, the study as themselves. This might have contributed to making a better connec-
group children's performance improved significantly in two attention tion and feeling of companionship between the child and the therapist.
components: complex attention and tracking tasks showed significant Ultimately, an individual approach to motivation was essential to
improvement in various aspects. Van't Hooft et al. [49] previously also enhance the positive intervention effect and see the best possible
described positive change in children after rehabilitation in complex at- improvement levels.
tention tasks, in contrast to the simpler reaction time tests. A better out- Furthermore, it was subjectively noticeable that the children's moti-
come in complex attention could show improved abilities to vation was also influenced by their parents' attitude toward training
concentrate on tasks, and to divide and shift attention between stimuli. sessions. If parents were less keen to participate in the regular meetings
Less commission errors may also suggest improvement in impulse and verbally explained their lack of motivation, their children also
control and behavior regulation, as commissions in tasks have been showed less acceptance with training. Educating parents about the
described as indicating impulsivity by rapid, but incorrect responses importance and outcome of rehabilitation facilitates cooperation and
[50]. Also, the tracking component of attention or tracking the compliance.
120 M. Saard et al. / Epilepsy & Behavior 67 (2017) 111–121

4.4. Limitations and future directions Declaration of conflicting interests

The study also has limitations. For one, the study group was com- We have no conflicts of interest to declare.
posed of children who lived in Tartu city or near Tartu, which means
that the group was not completely randomly chosen. Secondly, the Funding
information about the children belonging either to the study group or
waiting-list group was known to the therapist and this was not a blind This study was supported by the Estonian Science Foundation
study. Therefore, the results might have been affected by this to some (GARLA 9016) and by the Estonian Ministry of Education and Research
extent. Thirdly, the children who were below the normal intelligence TARLA 2695.
level were not included in the study, but the comparison of results
for intelligence tests between study and control groups was not Ethical approval
shown in detail. Also, typical for intervention studies, the sample size
was relatively small. Therefore, continued research is recommended The study was approved by The Research Ethics Committee of the
with a larger sample size. Still, it should be noted that the intervention University of Tartu 190T-21.
is a time-consuming and long-lasting process and therefore, resources
may be limited for conducting research with substantial sample sizes. Acknowledgements

5. Conclusions The work was done at the Department of Neurology and

Neurorehabilitation, Children's Clinic, Tartu University Hospital, Tartu,
Our multifaceted neurorehabilitation design with FORAMENRehab Estonia. The authors thank all the patients, control group children, and
is effective for children with epilepsy. Training specific attention com- their parents for their valuable contribution to this study.
ponents combined with individually tailored motivation and teaching
metacognitive strategies improved attention function in children with References
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