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Care for consequences in children treated for leukemia or brain tumor
Aukema, E.J.
Publication date
2013
Link to publication
Citation for published version (APA):
Aukema, E. J. (2013). Care for consequences in children treated for leukemia or brain tumor.
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Exploring the feasibility of
Neurofeedback training
as a cognitive intervention
for childhood brain tumor
survivors: a pilot study
E.J. AukemaM.Sc. A.Y.N. Schouten-van MeeterenM.d., Ph.d.
B.F. LastPh.d. M.h.M. BretelerPh.d. J. hogewegPh.d. M.A. GrootenhuisPh.d.
this manuscript has been resubmitted in the form of a brief report
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Abstract
Introduction: Childhood brain tumor survivors (CBTS) experience neurocognitive
deficits hindering learning for which neurocognitive interventions are needed. Neurofeedback training (NFT) is an effective intervention for children with Attention Deficit/Hyperactivity Disorder (ADHD) and could also be valuable for CBTS. This pilot study examines the feasibility of NFT in 9 CBTS.
Methods: Based on individuals’ quantitative electroencephalograms (QEEG’s) NFT
protocols were made and participants received 30 sessions NFT. Pre- and post NFT assessment consisted of neurocognitive tests and psychosocial questionnaires. Additionally, participants and parents were interviewed to explore their experiences with NFT.
Results: Nine CBTS (13-19 years old, time since end of treatment 2-16 yrs) completed
the NFT and no negative side-effects were reported, other than the amount of time needed to accomplish the intervention. NFT was evaluated as being enjoyable and recommendable for other survivors. Post NFT assessment revealed faster processing of information. In a post-NFT interview parents and survivors reported improvements in thinking, concentration and memory in daily life.
Conclusion: This pilot study indicates that NFT is a feasible intervention for CBTS and
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Introduction
Multimodal treatment strategies have substantially increased the overall survival rate of childhood brain tumor survivors (CBTS), but survival has not come without a cost [1]. Treatment is known to affect cognitive skills - processing speed, visuospatial skills, memory, sustained attention and executive functioning [2-6] - which are worsened by fatigue [7] and affect learning possibilities and psychosocial functioning [5, 8-10]. Therefore, the need for effective cognitive rehabilitation possibilities in this group of CBTS is high [2].
So far only a few cognitive rehabilitation programs have been developed and examined for their efficacy [11, 12]. Although some improvement was observed, intensity and compliance were reported to be a concern in those interventions and sustainability of the effects remains to be studied.
A neurocognitive intervention of increasing interest in children with ADHD, traditionally treated with pharmacological interventions (i.e. stimulant medication), is neurofeedback training (NFT) [13, 14]. Although CBTS differ from children with ADHD, CBTS seem to have inattention symptoms comparable to children with the Inattentive subtype of ADHD [15-19] and pharmacological interventions with stimulant medication (such as methylphenidate) improve attention functioning in CBTS [16, 20-23]. As such the effectiveness of NFT could be hypothesized in CBTS as well.
NFT is based on operant conditioning in which self-regulation of brain activity depicted by electroencephalogram (EEG) is taught [14]. Sitting behind a computer screen with electrodes on the scalp, the participant gets real time feedback on its brainwave activity. If the activity in specific EEG frequency bands alters in the desired direction the participant is rewarded. This reward can be given by means of a video or a sound or by gaining extra points when for example a computer game is used in the training [24]. Effects of NFT seem lasting as they generalize into everyday life through developed skills for self-regulation of brain activity by improving neuronal function [14, 24]. Studies in children with ADHD found improvements of inattention and in reaction time after NFT [25].
Prior to study the effectiveness of NFT in a randomized control trial (RCT), we wanted to explore the feasibility of NFT in CBTS and these first experiences can be used to optimize a future controlled study design.
The present study is the first to explore the feasibility of NFT in CBTS in terms of 1) the possibility of making a NFT protocol based on the QEEG’s of CBTS with neurocognitive deficits, 2) the effort and experiences of patients and parents with the NFT and 3) objective and subjective changes in daily life. We hypothesized that NFT, a validated treatment for ADHD, would also be a feasible training for CBTS in need of cognitive rehabilitation.
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Methods
Participants and procedure
Potential participants with neurocognitive deficits were recruited from an earlier study in our center [26]. Inclusion criteria for participation in this pilot study were: 1) being treated for a brain tumor, 2) current age of the survivor between 8 and 20 years, 3) at least 2 years after stop of treatment, and 4) parent-reported neurocognitive deficits. Exclusion criteria were: 1) deafness or blindness, 2) use of anti-epileptic medicine, and 3) use of methylphenidate. This pilot study was approved by the medical ethics committee of the Academic Medical Center of Amsterdam.
Sixteen survivors met the criteria for participation and the parents and/or survivors were first contacted by phone and then received additional information about the procedure and consequences of study participation and informed consent by mail. After consent, pre-assessment consisted of an intelligence test, neurocognitive tests, psychosocial questionnaires and a quantitative EEG (QEEG) [14] from which a NFT protocol was formulated by NF experts. Thereafter the participants received 30 sessions of NFT in training centers close to the participants’ place of residence. Within 5 weeks after the last training session, the neurocognitive tests and the psychosocial questionnaires were completed for the second time. This post-assessment was extended with an interview with both the CBTS and the parents exploring the effort, experiences with NFT and perceived changes in daily life. Open questions were used to prevent leading questions.
QEEG and NFT protocol and training
EEG data acquisition was based on 28 channels with scalp electrodes placed at 25 locations according to the international 10-20 system. The power was calculated in several frequency bands: delta (1.5-3.5 Hz), theta (4-7.5 Hz), alpha (8-13 Hz), alpha 1 (8-11 Hz), alpha 2 (11-13 Hz), SMR (12-15 Hz), beta (14.5-30 Hz), beta 1 (14.5-20 Hz), beta 2 (20-25 Hz) and beta 3 (25-30 Hz). Data were transformed to the normal distribution (in Z-scores) and compared with the norm database [27]. The objective of each individualized NFT protocol was to normalize the highest abnormal (high and or low) EEG activity to normal EEG activity. This is a standard procedure in the clinical practice of NFT centres [28].
Various studies (e.g Clarke 2002) suggest that different neuroanatomical systems are involved in cognitive functioning that can be distinguished by EEG measures[29]. As for example, Clarke et al. found different EEG clusters in studying the EEG activity of boys with the diagnosis of ADHD showing cortical hypoarousal (increased theta activity) or deficiencies in alpha and beta activity [30].
During a period of approximately 15 weeks participants received 2 NFT sessions a week. A session consisted of various intervals of training with eyes open or eyes closed, with pauses in between. In total a NFT session took approximately 45 minutes to 1
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hour. This includes setting up the computer and pasting the electrodes onto the head of the participant. The participant was told to sit behind the computer screen where the video or music plays whenever change in brain activity is measured in the desired direction. By continuous real-time feedback on their brainwave activity participants can learn to gain self-control over physiological functions. Changes in the desired direction based on the NFT protocol were rewarded by means of a video or sound that starts playing when a change in brain activity was measured by electrodes on the scalp [14].
Measures Patient characteristics
Individual patient data on gender, date of birth, and medical information including date of diagnosis, tumor type and type of treatment were gathered from the medical files.
Neurocognitive tests
At baseline intelligence was assessed to describe the cognitive functioning of the participants using the Dutch version of the Wechsler Intelligence scale for Children (WISC-III-NL) [31] or the Adults Intelligence Scale (WAIS-III) [32].
The neurocognitive tests assessed (1) Processing speed: processing speed factor (PSF - WISC-III [31] or WAIS-III [32], reaction time (Baseline Speed, Amsterdam Neuropsychological Tasks (ANT) [33]), and fine motor functioning and speed (Purdue Pegboard [34]); and (2) Attention: sustained attention (SA-DOTS, part of the ANT) [33], and selective attention (Stroop-colour and Word Test [35, 36]). All results were compared to age-norms and transformed in Z-scores.
Psychosocial questionnaires
Psychosocial questionnaires consisted of the Strength and Difficulty Questionnaire (SDQ: using the subscales Hyperactivity/Attention deficit and Total problems) filled out by parents [27], and the Self-perception profile for Adolescents filled out by the CBTS (using the School performance scale and the Total self perception scale [37]).
Interviews Evaluation of NFT
In the interview questions were asked about the effort (duration and frequency of the training, school and/or work absence) and experience with the actual performance of the training sessions (tiring, enjoyable and /or recommendable to others). Examples of these questions were “How do you perceive the amount of school and or work absence?” or “Would you recommend the training to other survivors?” The responses to these questions were categorized by the first author and an independent
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psychologist in a positive answer (for instance: “Yes I would recommend it to others”, a neutral answer (for instance: “I don’t know or I don’t have an opinion about it”) or a negative answer (for instance: “It took too much time to complete the NFT”).
Perceived changes in daily life
Perceived changes in daily life (categorized in cognitive, social-emotional, physical and school functioning) and more specific questions about cognitive functions (attention and concentration, speed of processing and thinking, and memory) and physical functioning (energy, sleep patterns and headache) were asked. Examples of these questions were “Have you noticed any changes in daily life or haven’t you?”, “Have you noticed any effect of the NFT regarding concentrating at school, paying attention in a busy environment, doing two things at the same time or haven’t you?” The responses to these questions were marked as positive (for instance: “Yes I noticed differences”), neutral (for instance:”I did not notice any change in remembering”) or negative (for instance: “I have less energy than before”).
Data Analysis
This pilot study was designed to investigate the feasibility of NFT in a group of CBTS. No group results were analyzed because of the large variability in personal and medical characteristics of the participants, the small number of participants and the explorative nature of this study. QEEG data were described in Z-scores based on the norm group [38].
All results but the intelligence scores were changed in Z-scores (Mean=0, SD=1) and compared to the norm groups of the tests. Meaningful changes within the individual CBTS regarding their neurocognitive and psychosocial outcomes were determined by reliable change index scores [39]. A reliable change index score is defined as the individual’s score before the intervention minus their score after the intervention divided by the standard error of the difference. Based on the test-retest reliability and the standard deviation of the test, the standard error of the difference can be estimated, using the formula SD √ (2-2 Rtt) (SD is standard deviation, Rtt is test-retest reliability). A one-tailed significance level of 5% is used to decide whether the change in score is significant. If the reliable change index is >1.65, it can be assumed that this is a significant change [39].
Answers of the interview were categorized in a positive, neutral, or a negative answer by 2 clinical psychologists and an inter-judgement correlation was calculated to analyse the agreement of the categorisation.
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Results
Participant characteristicsNine of the 16 CBTS (response rate 56%) who met the inclusion criteria participated. Non-participants considered NFT too time consuming with an uncertain outcome and therefore refused participation. It is however notable that all survivors and parents wanted to be informed about the outcome of the study.
CBTS characteristics are depicted in Table 1. Six CBTS were medulloblastoma survivors, who received craniospinal irradiation which is known to hamper speed of processing. Most CBTS (mean age 17.0 yrs, mean interval from end of treatment 8.6 yrs) complained about being tired or having sleep problems (n=8), needing more time in thinking, processing of information and reacting (n=5) and having memory problems (n=5). Other complaints were attention problems (n=3) and dyslexia (n=3).
QEEG and NFT protocol
The QEEG profile of the CBTS showed increased or decreased EEG frequency bands compared to norm data and QEEG profiles were diverse. Most frequent patterns were: increased coherence O1-O2 in alpha, theta or beta (n=3), decreased alpha power (n=4), decreased beta 1 eyes open (n=3), or increased beta 1 (n=2). Based on the QEEG data, nine NFT protocols were developed with the objective to normalize the highest abnormal (high and or low) EEG activity to normal EEG activity [28].
Evaluation of the NFT: interviews
The inter-judgement correlation showed to be on average (Spearman’s r=0.86). Eight participants completed 30 sessions of NFT. Only one participant completed
Table 1: Characteristics of the CBTS (N = 9)
Abbreviations:
Fem= Female; EOT= End of treatment; Cran= Craniopharyngeoma; Med=Medulloblastoma; Astr= Astrocytoma; Hem= Hemangioblastoma
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29 sessions due to the holiday season. Most participants trained twice a week, either during or after class in a NFT center nearby. NF trainers noticed increased tiredness in CBTS, which reduced the mean training time approximately 30 minutes instead of the usual 45 minutes.
Table 2 shows the experiences reported in the interview by the participants and their parents. In the interviews, CBTS evaluated the effort and the participation in NFT mainly neutral or positive. Parents of CBTS were negative about traveling time to the training centre, duration and frequency of the training, and absence of school. However, most CBTS and parents would still recommend NFT to others.
Neurocognitive tests and psychosocial outcomes
Pre-assessment showed that the level of intelligence (mean FSIQ=83.8, SD=14.9) was lower than average, varying from 61 and 112, and showed deficits in processing
Table 2: Subjective evaluation of NFT reported by participants and parent(s)
Abbreviations:
s = self (participants), p = parent(s); n/a = data are not available, = means neutral; + means positive; - means negative judgement
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speed and sustained attention (Table 3). In general, psychosocial functioning (including attention problems) was rated in the normal range by parents and CBTS. At post-assessment, 7 out of the 9 CBTS showed improvement on at least one neurocognitive outcome compared to their pre-assessment scores based on the reliable change index method (Table 3). Processing speed improved in 6 CBTS: PSF improved in 2 CBTS; reaction time in 6, and fine motor speed of the non-dominant hand improved in 3 but decreased in 1 CBTS. Sustained and selective attention remained stable in most CBTS but improved in 1 respectively 2 CBTS.
Six CBTS rated a better psychosocial outcome compared to pre-assessment. Improvements were found on parent-reported behavior in 4 CBTS: total behavior (3 CBTS) and hyperactivity/attention deficit (1 CBTS). Improvement on self-competence was found in 3 CBTS: total self-self-competence (2 CBTS) and self-competence about school-performance (2 CBTS). A decrease in self-competence (School-performance) was found in 1 CBTS.
Table 3: Neurocognitive and psychosocial functioning of CBTS (pre-and post NFT assessment)
Abbreviations:
FSIQ= Full scale IQ; VIQ= Verbal IQ , PIQ=Performal IQ; Proc Sp=Processing speed; PSF=Processing speed factor; RT=Reaction time; dom=dominant hand; ndom=nondominant; FM= Fine motor functioning and speed; SDQ= Strenght and Difficulty Questionnaire; Total probl= Total problems; Hyper/ atten=Hyperactivity, attention deficit; Self comp=Self competence
All (but IQ scores) are presented in Z-scores: mean=0, SD=1; -1=a worse, +1 SD=a better score 1 = WISC/WAIS-III-NL; mean=100, SD=15
* = significant positive difference between pre and post assessment based on reliable change index scores # = significant negative difference between pre and post assessment based on reliable change index scores / = did not fill in questionaire
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Perceived changes in daily life: interviews
The inter-judgement correlation showed to be on average (Spearman’s r=0.73). Positive changes in daily life were reported by CBTS (n=9) and parents (n=7). Cognitive improvement, e.g. faster processing of information and clearer thinking (n=7), better attention (n=6) and better memory (n=3), was reported most frequently (Table 4). Improvement in physical functioning, consisting of more energy (n=4), fewer headaches (n=3) and better sleep (n=2), was reported as well. CBTS did not report worsening of symptoms.
Discussion
Children with ADHD of the Inattentive subtype have comparable attention problems to those of CBTS [16, 19], and benefit from NFT [13, 14]. The question arises whether NFT would be beneficial for CBTS as well. Prior to investigating the effectiveness of NFT in a randomized control trial we explored the feasibility of NFT in CBTS.
Our first experiences with NFT in 9 CBTS are positive. All participants, except 1 who missed 1 session for holidays, completed the 30 sessions of NFT, which illustrates the high compliance, given the outpatient character of this study and compliance was
Table 4: Subjective changes in daily life reported by the participants and their parent(s)
Abbreviations:
Soc/emo = social emotional; s = self (participant), p = parent(s); n/a = data are not availalbe = neutral; + positive; - negative; +,- positive and negative judgment
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of concern in other types of recently developed rehabilitation programs [11, 12]. In evaluating the training, participants and parents judged the NFT positively, despite the required effort.
It was possible to create NFT protocols based on participant’s QEEG’s. However, the QEEG profiles of the CBTS showed great variety and did not resemble those profiles often seen in children with ADHD for which standard NFT protocols have already been developed [14, 28, 40]. Therefore individualized NFT protocols were needed. This seems in line with the recent study where attentional problems in CBTS were not fitting the ADHD symptoms according to the ADHD DSM-IV scale [17]. After NFT we found indications for improvements on neurocognitive functioning in most CBTS, especially in processing speed. We found these improvements on objective standardized neurocognitive tests, which remained after correcting the data for learning effects [39]. These improvements are remarkable as CBTS are known to decline in neurocognitive functioning in time. Nevertheless, placebo- or Hawthorne effects in this pilot-study should be taken into account.
Besides improvements in the majority of test scores, an increased speed of processing was also reported in the interviews. This is promising, since slowness seems to be the core deficit in CBTS which hampers the acquisition of new skills and knowledge [41]. The 2 CBTS who did not seem to benefit from the NFT (participants 3 and 5, Table 1) remained stable on all outcomes. Having more energy and less fatigue were additional changes in some participants. Fatigue is a common late effect after cancer treatment which hampers daily functioning and is difficult to improve [7]. Improvement in speed of processing and fine motor speed could be an explanation for the higher energy level in daily life. Additionally activating neuronal arousal through NFT could also have a positive effect on the energy level.
Due to variation in personal and medical characteristics between the CBTS in this pilot study, data are presented as individual scores. Further research in NFT is currently ongoing in a double blind randomized fashion including a control group to correct for non-specific training and possible placebo-effects [14]. Examining the potential effect of medical characteristics in a larger patient sample could be useful in understanding which patients could benefit from the intervention. Also monitoring of school results is highly recommended, since the effect of rehabilitation training is often difficult to distillate from mere neurocognitive parameters [42, 43]. The effect of NFT is expected to sustain for a long time, but sustainability of the possible effects in CBTS remains to be studied [24]. Finally, travelling time, fatigue of the patients and cost-effectiveness should be taken into account.
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Conclusion
This pilot study depicts NFT as a feasible intervention for CBTS. The first experiences with the training were judged positive by CBTS and their parents. Furthermore, the neurocognitive changes point in a positive direction. Further research is recommended preferably in a randomized control trial to assess whether NFT is truly an effective intervention for CBTS suffering from neurocognitive deficits.
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