Methods

Patient cohort

The Bath specialist paediatric CFS/ME service covers a region in the south west of England with a population of some 400 000 children aged 5–19 years (2001 census). The service also offers assessment and treatment to children from out of the region who cannot access specialist services. More than 150 children and young people are assessed and treated each year. Children are assessed and offered treatment in outpatient clinics unless they are too severely affected to attend clinic, in which case they are seen at home. All children referred into the service complete the following inventories: 11-item Chalder fatigue scale;13 the Short Form 36 physical function subscale to measure functional disability;14 the Hospital Anxiety and Depression Scale15 (if they are over 14 years old); the Spence Children’s Anxiety Scale,16 a pain visual analogue scale, and a single item inventory that asks about the percentage of possible attendance at school. At assessment children are routinely asked about those symptoms used in the adult Centres of Disease Control and Prevention definition for CFS/ME in adults,17 as well as common symptoms in CFS/ME as described in the Royal College of Paediatrics and Child Health guidelines.3 This includes the presence or absence of memory problems.

Children with CFS/ME who were between the ages of 6 and 16 years, and who described a problem with memory or concentration were recruited consecutively over a period of 6 months (May–October 2007). The problem with memory or concentration was identified using a symptom check list and an item from the Chalder fatigue scale specifically about memory and attention problems.

Ethical permission for the study was granted by the North Somerset and South Bristol NHS Research Ethics committee. The study was also approved by the Research and Development Department of the Royal National Hospital for Rheumatic Diseases, where the Paediatric CFS/ME service is based.

Qualitative memory and attention semistructured questionnaire

Children, their parents and teachers were each given a questionnaire asking whether the child in question found it hard to remember things or had difficulty concentrating. Both questions required a yes/no response. If a yes response was given they were asked to give further details of what the child found difficult to remember or concentrate on. Thematic analysis was used to analyse the qualitative data from this questionnaire by two independent researchers.

Neuropsychological assessment

Table 1 describes the tests used, what they measure and how many children were used to derive normative data for each test. Subtests were chosen from a battery of neuropsychological tests commonly used in children and were administered using standard procedures. Testing was conducted at a table in a quiet room in the child’s home. In some cases a parent was present for the testing procedure and remained silent throughout.

Raw scores of all the psychometric tests were converted into age-scaled scores and one sample t tests (two-tailed) used to compare the mean psychometric scores with normative data.18

The data were analysed using STATA 9.2 for Windows.

Results

Patient characteristics and missing data

Twenty-five children were invited to take part in the study; of these 18 were new patients and seven were patients who were seen at follow-up. Out of the 25 children, three did not return their consent forms, one became too ill to begin the testing procedure and one decided not to take part, leaving 20 children to take part in the study.

Not all the tests were completed for each child. One child was unable to complete the zoomap subtests due to circumstances unrelated to the test. One child misunderstood the instructions for the TEA-Ch subtest “Sky Search DT” and in accordance with test instructions their results for this test were invalid. Nineteen children completed the semistructured questionnaire used for the qualitative study. All parents and five teachers completed the questionnaire.

Table 2 compares the newly assessed children who had memory testing with those (N  =  42) newly assessed by the service in the same period, who did not have testing. There was no difference in terms of age, sex, fatigue, anxiety, pain, physical functioning, total number of symptoms, time at school and time to assessment. In addition, there was no difference between new and follow-up patients recruited for the study or between those that did and did not drop out in terms of fatigue, anxiety, pain, physical function, number of symptoms, school attendance, clinic latency and age at clinic.

Out of the 20 children tested, 19 were right handed. There were 13 girls; age range 8–16 years (mean 13.5, SD 2.6). None of the children had known problems with sight or hearing, which was confirmed with practice items completed at the start of testing designed to elucidate problems with sight or hearing that would adversely affect performance.

Eleven children elected to have their parents present for testing. The mean processing speed and focussed attention scores in these children were lower than the remainder (respective mean differences 4, 95% CI 0.8 to 7.1 and 2; p = 0.017, 95% CI 0.5 to 3.5 p = 0.011) suggesting that they took longer to process information and had more difficulty focusing their attention. There were no significant differences in any of the other tests. All parents remained silent throughout testing.

Qualitative memory and attention semistructured questionnaire

Four final themes were agreed on by the two researchers analysing how the children, their parents and teachers described the difficulties the children experienced with concentration and memory. These four themes were named: focussed attention; sustained attention; recall and stress.

Focussed attention

Parents, teachers and children described problems with attention: specifically attending to external cues, such as conversations or instructions. The children, their parents and teachers gave examples of difficulties with concentrating when information is being given, especially instructions and processing language:

“When someone is talking to me I find it hard to concentrate on what they are saying” (Child 20)

“All the stuff I’ve been told in class and at home it goes everywhere and I forget it” (Child 8)

“My mind wanders all through (sic) I am listening, I just don’t concentrate very well, it doesn’t sink in” (Child 5)

Parents report that their children find instructions difficult to understand and need to be told things more than once:

“[she] finds it harder to grasp new things and requires several explanations” (Parent 10)

The children described that they were often distracted and their “minds wandered” or they “lost track” of instructions and information given to them. They reported difficulties with getting started with a task or mentally preparing to listen.

“School work is a struggle (sometimes) because I can’t concentrate on the subject properly or get easily distracted” (Child 15)

Sustained attention

Parents, teachers and children described problems with sustained attention. Essentially this was about the children being able to maintain their mental stamina and successfully complete tasks over time. Twenty-four of the respondents reported that time was a factor in the span of concentration and that the children could not maintain concentration for long:

“[He] finds it hard to concentrate on anything for more than 10–15 minutes” (Parent 2)

In particular, it was noted that their concentration span was shorter than before the illness, they lacked mental stamina and quickly lost interest in any task requiring even limited concentration:

“She finds it difficult to concentrate on homework that requires her to spend a longer period of time to complete” (Parent 10)

Also described were difficulties with processing information, such as reading and writing:

“Difficult tasks for example tests, both written or audio” (Parent 5)

“I find reading quite hard now, I was a former book worm!” (Child 15)

Recall

Parents, teachers and children described problems with recall; the difficulty the children have with remembering specific information such as things they may have learnt, or where they might have put something. Child 6, for example, pointed out that she often forgets where she has put her belongings:

“[I forget] where I’ve put stuff—eg, shoes, handbag etc” (Child 6)

In addition respondents also made the point that the children often find it difficult to retrieve information and then relay it to other people:

“[I forget] what I am going to say, just as I start to say it” (Child 20)

Recalling information seems to be part of a cyclical process. The children describe experiencing problems laying down memories because they cannot concentrate on the input:

“When someone says something to me or tells me to go and do something if I don’t do it right away I will forget about it” (Child 12)

Therefore when they are required to retrieve information they find that it is not there, or they have difficulty locating the information:

“I can’t remember things that have just happened” (Child 15)

Stress

The experience of stress was commonly reported in one way or another by the respondents. The descriptions of stress fitted into two categories: psychological and behavioural.

Psychological effects that were mainly frustration:

“I get frustrated when my teacher talks too much” (Child 8)

“She gets frustrated when she can’t do what she used to” (Parent 3)

Behavioural reactions to stress were described by the parents and teachers:

“He gets a lot more irritable and fidgety when doing things” (Parent 1)

“He also gives up easily if he can’t easily do the task” (Parent 18)

Neuropsychological assessment

This method of assessing the memory and concentration problems of children with CFS/ME was found to be feasible and was acceptable to the majority of the children who took part. Only one child was unable to complete the testing due to circumstances unrelated to the test. All the children had two test sessions over two consecutive days, and testing lasted approximately 30 minutes inclusive of breaks each day. Parents found the testing useful and all parents asked for reports of the testing, which they used in discussions with schools over the problems their children experienced.

Table 3 summarises the results from two-tailed t tests comparing the children’s scores with the normative data. Scores for sustained attention (mean 8.1, 95% CI 6.3 to 9.9), switching attention (7.5, 5.5 to 9.4), divided attention (6.9, 5.5 to 8.2), auditory learning (8.2, 6.8 to 9.6) and immediate recall (8.7, 7.3 to 10.0) appeared lower than the normative mean of 10. These results are consistent with the qualitative data.

Discussion

We have shown that it is feasible and acceptable to do a battery of neuropsychological testing in children with CFS/ME. Only one child was unable to complete the testing. All parents found the testing acceptable.

Children with CFS/ME, their parents and teachers describe difficulties with attention, sustained attention and remembering specific information (or recall). These difficulties were frequently described as being associated with stress. The problems described are consistent with the neuropsychological test results, which indicate problems with sustained attention, switching attention, divided attention and auditory learning.

The scores for processing speed and focussed attention for children who had a parent present during testing were lower than for children who had completed the testing alone. It is unclear whether this means that having the parent present was detrimental to the child’s performance or whether the children who wanted their parents present had more problems with processing speed and attention.

Attention

The most common problems were in divided attention and switching attention. The mean for divided attention was more than 1 SD below the normative mean and is therefore clinically significant. Children with a score below 7 would be considered to have a clinically significant problem. In the divided attention test, children are asked to do two previous tests (the Sky search and Score!) simultaneously. Performance on this task measures the ability to sustain and divide attention by attending to two things at once. The low mean for the switching attention subtest might suggest that the children in this study have slower than average information processing as the score depends on the time it takes to complete the task. However, the mean score for the symbol search subtest, which directly tests processing speed, is not significantly different from normative data. This could be because the symbol search test only requires the children to do one thing continually; locate a symbol within a group of five symbols, whereas the test for switching attention requires the children to do two things continually; count one way until encountering an arrow then count the opposite way. In addition, some children appeared to have a problem with sustained attention, which suggests that concentrating for extended periods of time could be difficult.

The auditory learning task involves learning word pairs, the lower score compared with normative data means that children with CFS/ME required more trials to learn the auditory information. It is probable that the difficulties that these children experience will have a negative impact on their education.

An impairment in attention may be the basis for other cognitive difficulties in CFS/ME.6 Before information is relayed to memory, it is necessary to attend to it, and the data suggest that, rather than problems with manipulating information (in working memory), recalling after a delay (in long term recall), or retrieval (as recognition memory scores were in the normal range), the group with CFS/ME has difficulty attending to and encoding information. Once information has actually been stored, it is relatively well recalled, as demonstrated by the normal scores on delayed recall, and there is little evidence of retrieval problems suggested by the delayed recognition scores.

Strengths and limitations

This is the first study to investigate memory and concentration problems in children with CFS/ME. The mixed methodology enables us to understand more about the quantitative results. Children with memory or attention problems were recruited prospectively from a large unselected group of children and young people attending a paediatric CFS/ME clinic with a high response rate. However, as the children were selected from a regional specialised service, it is possible that the children described are more severely affected or may have had lower premorbid levels of functioning than those attending a general paediatric clinic, and the results may not be generalisable to general paediatric or community services. In addition, children were only recruited if they presented with memory problems so the results cannot be generalised to those without.

In this feasibility study 20 children were tested and only a small number of neuropsychological tests were carried out in order not to fatigue the children. As CFS/ME is considered a heterogeneous condition, it is possible that the memory and concentration problems are different in different children at different ages. It will clearly be of interest to study this in a larger group without selecting for those with memory problems using a case–control design.

Results in context with other studies

Previous studies have described problems with divided attention in adults,19 which was thought to be due to slower information processing affecting tasks that require divided attention.20 Deficits in the more demanding tasks in central executive functioning and working memory have been described in adults, in particular resistance to interference and efficient switching between processing routines.21 None of the problems described have convincingly been shown to be related to the severity of fatigue, but some are associated with low levels of physical activity.22

There is evidence to suggest that adults with CFS/ME have impaired auditory learning compared with healthy controls11 and impairment in immediate free recall of auditory information.22 Michiels et al19 investigated verbal memory in more detail and showed that the poor performance of adult patients with CFS/ME was due to poor initial storage rather than retrieval failure. Both the qualitative and quantitative results from the current study seem to support this.

Conclusions

This is the first study to demonstrate that children and young people with CFS/ME experience problems with focussed attention, sustained attention, recall and stress. Quantitative analysis is consistent with the problems described by children, their parents and their teachers.

These problems are particularly likely to affect children with CFS/ME when they are trying to do two tasks at the same time such as doing their homework and keeping a track of time, or reading and listening to music at the same time. It may be appropriate for young people with CFS/ME to have access to visual aids, be allowed extra time to complete work including frequent breaks.

Paediatricians need to be aware of these problems when they assess children and plan their rehabilitation, particularly when they are supporting children accessing appropriate education.