Mental Fatigue and Attention Problems Due to Brain Injury

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    Brain Injury, December 2009; 23(1314): 10271040

    Mental fatigue and impaired information processing after mild andmoderate traumatic brain injury

    BIRGITTA JOHANSSON, PETER BERGLUND, & LARS RONNBACK

    Department of Clinical Neuroscience and Rehabilitation, Institute of Neuroscience and Physiology, The Sahlgrenska

    Academy, University of Gothenburg, Gothenburg, Sweden

    (Received 4 March 2009; revised 8 October 2009; accepted 18 October 2009)

    AbstractPrimary objective: Mental fatigue is a common symptom after brain injury. Its mechanisms are not fully understood andit has been difficult to find an objective way of measuring it. The aim was to compare cognitive tests with a newself-assessment questionnaire about mental fatigue.

    Methods and procedures: Individuals reporting mental fatigue for 6 months or more after mild traumatic brain injury (MTBI)or traumatic brain injury (TBI) and controls were assessed for subjective fatigue, information processing speed, workingmemory and attention. Depression and anxiety were also assessed in the individuals with brain injury.Results: Individuals with MTBI or TBI reported significantly more problems with mental fatigue and related symptoms thancontrols. A significantly decreased information processing speed (digit symbol-coding, reading speed, trail making test) wasfound in those on sick leave due to MTBI or TBI, compared to controls. Divided attention was affected to a lesser extentand no effect was detected on working memory.Conclusion: Mental fatigue after MTBI can last for several years. It can be profoundly disabling and affect working capacityas well as social activities. Subjective mental fatigue following brain injury is suggested to mainly correlate with objectively

    measured information processing speed.

    Keywords: Mental fatigue, TBI, MTBI, self-assessment questionnaire, information processing speed, working memory, digit

    symbol-coding, reading speed, TMT

    Introduction

    Fatigue is a common symptom after both a mild

    traumatic brain injury (MTBI) and traumatic brain

    injury (TBI). Mental fatigue is characterized by

    concentration and memory difficulties as well as

    increased fatigability after mental activities, withdepletion of energy which can take days to recover

    from. For most individuals the problem disappears

    within a year, but for some, mental fatigue becomes

    a chronic problem that affects daily life. The

    mechanisms that cause mental fatigue are not fully

    understood and no clear treatment guidelines have

    been developed. Therefore, it is important to find

    appropriate assessment methods to increase knowl-

    edge of mental fatigue.

    Concern about the different aspects of mental

    fatigue has been addressed for neurological diseases

    and injuries [1] and an investigation revealed thatit is the most common problem following TBI, as it

    can last for many years and influences daily activities

    [2]. One third of the patients who suffered from

    MTBI complained of severe fatigue at 6 months as

    well as a decrease in physical and social activities [3],

    while 40% complained of headache and fatigue

    Correspondence: Dr Birgitta Johansson, Department of Clinical Neuroscience and Rehabilitation, Institute of Neuroscience and Physiology, The Sahlgrenska

    Academy, University of Gothenburg, Per Dubbsgatan 14, 1tr, SE 413 45 Gothenburg, Sweden. Tel: 46-31-34210 00. E-mail: birgitta.johansson2@

    vgregion.se

    ISSN 02699052 print/ISSN 1362301X online

    2009 Informa Healthcare Ltd.DOI: 10.3109/02699050903421099

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    1 year after concussion [4]. After 5 years, 73%

    reported still having a problem with fatigue, which

    affected them in everyday life [5]. Even after 10

    years, fatigue was still present, irrespective of injury

    severity [6]. Improvement was reported during the

    first year, after which it was limited [7]. Fatigue after

    brain injury has a significant effect on well-being and

    quality of life and is suggested to be due to the brain

    injury, as it cannot be explained as an effect of

    depression, pain or sleep-disturbance [8]. In addi-

    tion, the degree of fatigue is not related to the

    severity of the injury, age or time since injury [9, 10].

    Mental fatigue is central to many neurological

    disorders and biological models have been proposed

    as a means of understanding pathophysiological

    mechanisms. Chaudhuri and Behan [1] formulated

    a hypothesis suggesting that metabolic and structural

    lesions that disrupt the usual process of activation

    in pathways interconnecting the basal ganglia,

    thalamus, limbic system and higher cortical centreare implicated in the pathophysiological process

    of central fatigue. Another hypothesis proposed

    that functions of the glial cells in the brain are out

    of balance [11, 12]. Inflammatory activity with

    microglial activation and the production of cytokines

    could be responsible for an attenuated astroglial

    fine-tuning and support of the neuronal glutamate

    signalling, which is of the utmost importance for

    information processing in the brain. In addition,

    other systems have been found to be affected.

    Recent research results demonstrate that there is

    an imbalance in the regulation of the hypothalamus-

    hypophysis-adrenal cortex (HPA)-axis, which isunder the control of the excitatory neurotransmitter

    glutamate [13]. It was also shown that glutamate can

    activate the amygdala to release the corticotropine-

    releasing factor [14], which in turn can lead to

    increased glucocorticoid levels. Moreover, it has

    been suggested that genetic variation is

    important [15].

    It has proved difficult to relate cognitive functions

    such as attention and memory to mental fatigue

    [10]. However, mental fatigue theories suggest that

    cognitive activities require more resources than

    normal [16] and subjective assessment of fatigue

    has been found to correlate with complex selectiveattention [9] and information processing speed [17].

    Higher neuronal activity compared to controls

    during a mental activity may also indicate an

    increased cerebral effort after brain injury [18] and

    support for the theory above [16].

    There are a large number of different scales for

    assessing fatigue, of which several were designed

    for a specific disease [19] as well as for patients with

    brain injury [10]. This means that different scales

    report varying effects and accordingly it is difficult

    to conduct intervention studies due to the lack of

    validated tests [20]. The aim of this project was to

    find better ways to determine mental fatigue. Both

    subjective and objective measurements were used

    with the intention of more clearly identifying

    items associated with mental fatigue. A new self-

    assessment scale was employed for the subjective

    rating of mental fatigue and related symptoms [21]

    in combination with objective tests of information

    processing speed, working memory and divided

    attention.

    Method

    Participants

    The main purpose was to study subjectively reported

    mental fatigue and cognitive functions and not the

    frequency of mental fatigue. Participants with MTBI

    or TBI who were reporting long-term mental fatigue

    were recruited by means of an advertisement in alocal newspaper. Some subjects were also recruited

    by a Swedish patient association for people with

    brain injury and from the department of neurology at

    the Sahlgrenska University hospital. The inclusion

    criteria were MTBI or TBI with no other neurolog-

    ical or psychiatric illnesses, no dyslexia and hav-

    ing sustained the injury over 6 months prior to

    inclusion. All MTBI participants had been diag-

    nosed with commotion/concussion (ICD-10 S06.0).

    Participants with TBI were not differentiated

    between moderate and severe, but they all described

    a moderate-to-severe head trauma and had been

    hospitalized for varying lengths of time (months to ayear) and had received rehabilitation in specialized

    units. The subjects with MTBI or TBI had no

    motor complaints and all were living independently.

    Some were working full time, while others were on

    sick leave, most of them 100%, but some to a lesser

    extent such as 25, 50 and 75%. MTBI working full

    time were analysed separately, as it was assumed that

    they could give valuable information about working

    capacity and about severity of mental fatigue.

    Control participants with no history of head injury,

    no neurological disturbance or psychiatric illness,

    no limitation in working capacity and of similarage, education and gender were recruited from the

    general community. The study was approved by

    the regional Ethics Committee in Gothenburg. The

    participants gave their informed written consent

    before the assessment.

    Self-assessment of mental fatigue

    The self-reported questionnaire contains 15 ques-

    tions and was adapted from Rodholm et al. [22].

    The questions cover the most common symptoms

    occurring after brain injury [23, 24]. Each item

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    comprises examples of common activities to be

    related to four response alternatives (see Appendix).

    The rating is based on intensity, frequency and

    duration. Higher scores reflect more severe symp-

    toms. A rating of 0 corresponds to normal function,

    1 indicate a problem, 2 a pronounced symptom and

    3 a maximal symptom. It is also possible to indicate

    a score between the given alternatives (0.5, 1.5, 2.5).

    The intention was to construct an assessment scale

    with response alternatives that can help the subjects

    to be clearer and more consistent in their judgement.

    The questions concern fatigue in general, lack of

    initiative, mental fatigue, mental recovery, concen-

    tration difficulties, memory problems, slowness of

    thinking, sensitivity to stress, increased tendency to

    become emotional, irritability, sensitivity to light and

    noise, decreased or increased sleep as well as 24-hour

    variations. The construction of the questionnaire

    resemble the Comprehensive Psychopathological

    Rating Scale (CPRS) designed to measure changesin psychopathology over a short period [25].

    A clinical interview was performed based on the

    questions from the self-assessment scale as well as

    the CPRS to measure the presence of depression

    and anxiety. Participants with brain injury were

    also asked about changes in their leisure and social

    activities, both at home and outside the home

    according to the structured interview for the

    Glasgow Coma Scale [26].

    Neuropsychological tests

    The neuropsychological tests measured informationprocessing speed (the time required to execute

    a cognitive task within a finite time period) [27],

    attention, working memory, verbal fluency and

    reading speed, which are common problems after

    MTBI. The tests included were digit symbol-coding

    from the WAIS-III NI [28], measuring information

    processing speed. Attention and working memory,

    both auditory and visual, were measured by means

    of the digit span and spatial span [28]. Both tests

    included repetition of forward series of random

    numbers or blocks in order as well as in reverse.

    The verbal fluency test (FAS) measures the ability to

    generate as many words as possible beginning witha specific letter within 1 minute [29]. Parts A and B

    of the Trail Making Test (TMT) were administered

    according to the published guidelines [30] in order

    to measure visual scanning, divided attention and

    motor speed [31]. The test consists of a series of

    connect-the-circle tasks, part A with a numerical

    order of 125 and part B comprising letters and

    digits in alternating numerical and alphabetical

    order, which have to be completed as quickly as

    possible. In order to evaluate higher demands such

    as dual tasks, a series of new tests was constructed

    with three and four factors, respectively. The same

    number of circles (25) was used in all parts. The

    alternation between factors was similar to part B

    except for the fact that months were added in part C

    and both months and days of the week in chrono-

    logical order in part D. In the latter, the order of

    letters and digits was changed (A: 125, B: 1-A-2-

    B-3-C, C: 1-A-January-2-B-February-3-C-March,

    D: A-1-January-Monday-B-2-February-Tuesday).

    The reading speed was measured using the DLS

    reading speed test [32]. The participants were

    instructed to read the text silently and mark the

    correct word that corresponded to the meaning of

    the sentence from 36 evenly distributed parentheses

    containing three words, which serves as a check of

    reading comprehension. The whole text contains

    887 words and the time taken to read each page was

    recorded. The average number of words per second

    and page was measured. The native language of the

    healthy controls was Swedish, with the exceptionof one individual whose first language was English,

    but who had lived in Sweden for 10 years and

    spoke Swedish fluently. None of the healthy controls

    reported any reading problems or dyslexia. One

    MTBI participant reported dyslexia and was

    excluded from the analysis of reading speed.

    The assessment was made in the following order:

    self-assessment of fatigue, Trail Making Test, assess-

    ment by the examiner, i.e. a neuropsychologist or

    psychiatrist, of subjective fatigue, depression and

    anxiety, digit symbol-coding, digit span, spatial span,

    verbal fluency, reading speed and social function.

    The instruments were administered according to therespective published guidelines.

    Statistical analysis

    The self-assessment questions and binominal data

    were analysed by the non-parametric Kruskal-

    Wallis, Mann-Whitney and Chi-squared tests.

    Bonferroni adjustment was used after multiple

    comparisons. ANOVA, ANCOVA and regression

    analysis were employed for the parametric data and

    Bonferroni served as a post-hoc test. Spearmans

    rank correlation was used for the analysis of the

    subjective assessments and cognitive tests. Theinternal consistency reliability of the self-assessment

    questions was analysed by means of Cronbachs

    alpha. SPSS 16.0 for Windows was used for data

    analysis.

    Results

    Demographics

    The participants were divided into four groups;

    controls (Group 1), persons with MTBI in full time

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    employment (Group 2), persons with MTBI who

    were on sick leave (Group 3) and persons with TBI

    who were on sick leave (Group 4). As no statistical

    difference was found between the groups with

    different degrees of sick leave (25, 50, 75 or

    100%), they were therefore combined. Sick leaveof 100% was the most common. Demographic data

    are presented in Table I. More women than men

    participated in the study, but there was no significant

    difference in number of men and women between

    the healthy control and brain injured groups.

    A significant age difference emerged (F9.01,

    p

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    injury were found for reading speed, where group 2

    was faster than group 4, and for the TMT D, where

    group 2 was faster than group 3. Reading speed and

    digit symbol-coding were maintained at almost the

    same speed in both tests.

    No significant difference in auditory (digit span)and visual (spatial span) working memory for total

    and backward scores or visual span forward were

    detected between groups. The only significant

    difference was that group 3 scored fewer digits

    forward compared to the control group (p

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    significantly decreased their outdoor physical activ-

    ity, activity at home and even social life outside and

    in the home compared to MTBI working full time

    (all questions, p

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    one participant was assessed as being depressed.

    Aches and pain from the CPRS was above 0.5 in

    groups 3 and 4 and both increased and decreased

    sleep was reported (Figure 5).

    Discussion

    Mental fatigue after MTBI is a common problem

    and it often limits working capacity as well as the

    ability to participate in social activities. The present

    study aimed at investigating mental fatigue after

    MTBI or TBI and examining whether it can be

    related to cognitive functions. The authors wereunable to draw any conclusion about frequency,

    as the participants were recruited on the basis of

    reporting mental fatigue following brain injury.

    Subjective effects

    Subjects with MTBI and TBI, irrespective of work-

    ing capacity and severity, reported significantly more

    problems, both for total sum of scores and for all

    separate items in the self-assessment questionnaire

    compared to controls. In particular, mental fatig-

    ability, mental recovery and stress sensitivity were

    rated as high. The self-assessment scale includeditems with a high internal consistency and the

    questions also correlated significantly with each

    other. The scale was also relevant for different

    diseases [21]. This indicates that the core problem

    with mental fatigue comprise a broader spectrum

    of relevant items with either primary or secondary

    symptoms. The response alternatives may also make

    the self-reports more consistent and might have

    resulted in a more definite deviation from the healthy

    controls. Social and leisure activities were also

    affected and many of the participants had reported

    mental fatigue for many years. This is in agreement

    with other studies reporting that fatigue plays aprominent role in the lives of many people a long

    time after a TBI [25].

    Individuals with MTBI who were working full

    time did not change their leisure and social activities,

    although they rated their mental fatigue and related

    items on the same level as the participants with

    MTBI and TBI who were on sick leave. This may

    appear strange but, depending on their mental load

    during the day, subjects working full time might

    need to devote more attention to mental work and

    use more energy than is normal.

    Figure 3. The figure shows the significant negative correlation for

    the total sum score and digit symbol-coding (scale score used here

    is adjusted for age in accordance with the WAIS-III manual).

    Figure 4. Changes in leisure and social activities. Participants

    with MTBI who were on sick leave had significantly decreased

    their leisure and social activities both outside the home and at

    home compared to those with MTBI who were working full time

    (yesdecreased activity).

    Figure 5. Selected items from the expert assessment with CPRS

    and the self-assessment scale, showing median rating of depres-

    sion, anxiety, pain, sleep, mental fatigue and sensitivity of stress.

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    If they had the same mental effort, those on sick

    leave might become more easily fatigued, but sick

    leave or part time work probably helps them to

    conserve their energy, which is crucial, as today rest

    is the most important restorative factor for indivi-

    duals who suffer from mental fatigue. If, as

    suggested, mental activities require more cognitive

    or cerebral effort than normal [16, 18, 34], this

    would explain the similar subjective ratings among

    individuals with brain injury. Unlike in the case of

    those on sick leave, objective cognitive tests did not

    differ between healthy subjects and those with

    MTBI who were working full time and individuals

    with MTBI who were working full time read faster

    than both the MTBI group on sick leave and the TBI

    group and were faster in the TMT D than the MTBI

    group on sick leave, indicating a difference in injury

    severity.

    Objective effects

    Objective tests dependent on information processing

    speed were significantly impaired in the participants

    with MTBI on sick leave and the TBI group

    compared to controls. The working memory tests

    were not affected, with the exception of a significant

    decrease in group 3 on digit forward. Age correlated

    with digit symbol-coding [28] as well as with TMT

    A and B [35] and also with the total sum score for

    the self-assessment scale. However, after controlling

    for age (ANCOVA), significant differences remained

    for information processing speed. Regression analy-

    sis also indicated that age contributed to the varia-tion in self-assessment, but to a lesser extent than

    information processing speed. It is therefore sug-

    gested that information processing speed is a signif-

    icant factor related to mental fatigue in persons with

    MTBI and TBI, even when taking account of age.

    Age is thus significant in the self-assessment of

    fatigue and comparison between groups or interven-

    tion studies must control for age. The order of the

    tests cannot explain the slower information process-

    ing speed as due to fatigability during the test

    session, as the TMT, which was administered at the

    beginning of the assessment, was also characterized

    by decreased speed.The result is in agreement with studies that

    describe information processing speed as the most

    prominent function to be affected after brain injury

    [27, 36] and other neurological diseases [37, 38].

    Martin et al. [39] reported decreased information

    processing speed, but no effect on working memory

    after TBI. Reaction time increased when a more

    difficult information processing test was used [40].

    Spatial and digit span were in accordance with

    previous reports and spatial span forward and

    backward were on nearly the same level, while digit

    span forward was higher than backward among

    both healthy controls [41] and participants with mild

    injury [42]. The TMT results of parts A and B were,

    in the case of the control participants, close to the

    normative data presented by Tombaugh [35]. When

    compared with the WISC-III manual, the control

    group accords well with what is expected for a

    healthy group.

    Reading is a complex activity, involving automa-

    ticity, information processing speed and working

    memory. It is also an important activity in daily life

    and the most realistic test used in the present study.

    Reading is also commonly reported as tiresome and

    slow by patients after brain injury. However, it is

    usually employed for assessing dyslexia and not for

    testing cognitive disorders after brain injury or

    neurological diseases. This study demonstrates that

    reading speed can be a useful test for further

    exploration of the mechanisms involved in mental

    fatigue. TMT C and D, requiring a high load oninformation processing and divided attention, may

    also be valuable as this more complex and sensitive

    test makes it possible to capture milder cognitive

    deficits after brain injury with co-occurring mental

    fatigue.

    Aspects on mental fatigue and cognitive function

    A multi-factorial approach is most often used to

    describe the occurrence of mental fatigue. DeLuca

    et al. [43] discussed the problem of relating cognitive

    tests to fatigue and demonstrated increased neuronal

    activity after mental activity in patients with multiplesclerosis (MS). Similar results were also reported by

    Kohl et al. [18] for patients with TBI. Furthermore,

    a working memory task after brain injury was

    associated with increased neuronal activity [44].

    Azouvi et al. [16] proposed that mentally tiresome

    activities after brain injury were related to reduced

    resources and that patients with brain injury also

    described mental activity as more energy demanding

    than healthy persons. The same was reported after a

    divided attention task [34]. Moreover, a simultane-

    ous load on working memory that demands total

    control of the situation was more tiresome than an

    automatic activity [45]. The participants with MTBIwho were working full time also had a significantly

    higher total sum score of the self-reporting items

    than the controls, thus indicating that mental activity

    is more energy demanding than normally expected.

    The correlation here between mental fatigue and

    information processing speed is also in agreement

    with other studies [17, 46, 47]. Thumb pressing as

    an objective test of speed did not differ between

    control and TBI groups but was correlated with

    subjective fatigue [46]. Ziino and Ponsford [47]

    reported significantly slower performance on a

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    complex selective attention task and suggested an

    association with subjective fatigue. Furthermore,

    information processing improved after a repeated

    computerized test for healthy controls, something

    not found in the subjects with brain injury [17].

    Information processing speed is known to have an

    important influence on higher order cognitive func-

    tions such as working memory, episodic memory,

    executive function, reasoning, problem-solving,

    visual spatial as well as academic skills [27]. It is

    also important for many jobs due to the high

    demand on efficiency. A combination of subjective

    and objective measures is suggested for assessing

    mental fatigue, as it can provide a more specific

    assessment of the level of mental fatigue and also be

    of great value for estimating working capacity and

    the need for rest and rehabilitation.

    Depression

    Depression is common after brain injury but, withthe exception of one individual, the participants who

    voluntarily took part in this study were not found to

    be depressed. Furthermore, the results were not

    controlled for depression, as very low clinical ratings

    close to normal (0 or 0.5) of core items of depression

    were found for the participants with brain injury.

    As questions overlap between CPRS and the

    self-assessment of mental fatigue and related symp-

    toms, it was decided to show the depression and

    anxiety items separately in Figure 5. In the figure are

    also some of the symptoms from the clinical rating

    shown for a comparison with depression symptoms.

    Depression is more common among MTBI and

    TBI, but the inclusion criteria to this study and also

    the subjects being recruited voluntarily may have

    resulted in fewer depressed patients than would have

    been found in an epidemiological study. A mixture

    of fatigue, cognitive and depression items are often

    included in different depression scales and, together

    with other methodological discrepancies between

    studies, can explain some of the variation in depres-

    sion (from 677%) after brain injury [10]. Many

    studies report increased susceptibility to depression

    after brain injury, but the connection with mental

    fatigue is less clear. Fatigue after brain injury wassuggested to be an effect of the brain injury itself and

    not a result of pain, depression or sleep-deprivation

    [8]. Therefore, the authors hold that mental fatigue

    must be assessed thoroughly and needs to be

    separated from depression, as both symptoms are

    common and can co-occur but require different

    intervention strategies [48].

    Consideration of the study group and tests

    Time since injury varied between participants,

    but no significant correlation between cognitive

    function, subjective assessment and years since

    injury was found. In the case of 20 participants

    (34%), mental fatigue remained for more than

    10 years after the injury. This is in accordance with

    other studies, reporting long-term visual spatial and

    academic skill problems associated with fatigue after

    brain injury [24, 7, 49, 50], for up to 10 years,

    irrespective of injury severity [5]. Cognitive impair-

    ments are also common 10 years after brain injury

    [50].

    A high proportion of the participants in group 3

    had suffered two MTBI. Although it cannot be ruled

    out that their problems were worse, no significant

    difference was found when those reporting one

    and two brain injuries in group 3 were compared.

    No significant difference emerged between males

    and females for the included items in the subjective

    self-assessment scale for mental fatigue or in the

    cognitive tests. There were, however, more female

    participants in this study. One cannot draw anyconclusions about why more females volunteered

    but, in other studies, more women than men

    have reported subjective complaints after brain

    injury [8, 51].

    Limitations of the study

    The differentiation of brain injury was not based on

    commonly used classification systems, at it was

    not possible to collect case records from different

    hospitals. Furthermore, mental fatigue has not been

    related to severity of the injury and it was therefore

    decided to make this division into groups based onthe subjects description of the injury, if it has been

    classified as a MTBI or a more severe injury and also

    due to hospitalization. The estimation of depression

    and anxiety is based on a clinical interview according

    to CPRS and a self-assessment of depression

    and anxiety is not done here, but would have been

    valuable for adjustments and comparisons in statis-

    tical analyses. The items included in the self-

    assessment scale cover different areas such as sleep,

    sensory, emotional and cognitive domains, which

    all fit well together. Whether they are primary or

    secondary effects to the brain injury is unknown

    today, but will be important to explore in the future.In conclusion, mental fatigue after MTBI or TBI

    remains in many cases for a very long time and can

    be profoundly disabling, affecting working capacity

    as well as recreation and social activities. It is

    proposed that the self-assessment scale used here

    in combination with tests that primarily measure

    information processing speed and a high cognitive

    load on attention might make it possible to capture

    problems described by patients with mental fatigue

    such as reading, participating in discussions and

    activities involving an environment containing a

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    large amount of stimuli. Subjective mental fatigue

    after MTBI and TBI is thus suggested to primarily

    correlate with objectively measured information

    processing speed.

    Acknowledgements

    This work was supported by grants from The Health

    & Medical Care Committee of the Region Vastra

    Gotaland, Swedish Research Council, 21X-13015

    and from Fyrbodalinstitutet.

    Declaration of interest: The authors report no

    conflicts of interest. The authors alone are respon-

    sible for the content and writing of the paper.

    References

    1. Chaudhuri A, Behan PO. Fatigue in neurological disorders.Lancet 2004;363:978988.

    2. Ouellet MC, Morin CM. Fatigue following traumatic brain

    injury: Frequency, characteristics, and associated factors.

    Rehabilitation Psychology 2006;51:140149.

    3. Stulemeijer M, van der Werf S, Bleijenberg G, Biert J,

    Brauer JE, Vos P. Recovery from mild traumatic brain injury:

    A focus on fatigue. Journal of Neurology 2006;253:

    14321459.

    4. Holmqvist Andersson E. Mild traumatic brain injury. The

    impact of early intervention on late sequelae [dissertation].

    University of Gothenburg; 2004.

    5. Olver JH, Ponsford JL, Curran CA. Outcome following

    traumatic brain injury: A comparison between 2 and 5 years

    after injury. Brain Injury 1996;10:841848.

    6. OConnor C, Colantonio A, Polatajko H. Long termsymptoms and limitations of activity of people with traumatic

    brain injury: A ten-year follow-up. Psychological Reports

    2005;97:169179.

    7. Bushnik T, Englander J, Wright J. Patterns of fatigue and its

    correlates over the first 2 years after traumatic brain injury.

    Journal of Head Trauma Rehabilitation 2008;23:2532.

    8. Cantor JB, Ashman T, Gordon W, Ginsberg A, Engmann C,

    Egan M, Spielman L, Dijkers M, Flanagan S. Fatigue after

    traumatic brain injury and its impact on participation and

    quality of life. Journal of Head Trauma Rehabilitation

    2008;23:4151.

    9. Ziino C, Ponsford J. Measurement and prediction of subjec-

    tive fatigue following traumatic brain injury. Journal of the

    International Neuropsychology Society 2005;11:416425.

    10. Belmont A, Agara N, Hugeron C, Gallais B, Azouvi P.

    Fatigue and traumatic brain injury. Annals of Readaptive

    Medical Physics 2006;49:283288.

    11. Hansson E, Ronnback L. Altered neuronal-glial signaling

    in glutamatergic transmission as a unifying mechanism in

    chronic pain and mental fatigue. Neurochemistry Research

    2004;29:989996.

    12. Ronnback L, Hansson E. On the potential role of glutamate

    transport in mental fatigue. Journal of Neuroinflammation

    2004;1:22.

    13. Mathew SJ, Coplan JD, Schoepp DD, Smith EL,

    Rosenblum LA, Gorman JM. Glutamate-hypothalamic-

    pituitary-adrenal axis interactions: Implications for mood

    and anxiety disorders. CNS Spectrums 2001;6:555556,

    561564.

    14. Cratty MS, Birkle DL. N-methyl-D-aspartate (NMDA)-

    mediated corticotropin-releasing factor (CRF) release in

    cultured rat amygdala neurons. Peptides 1999;20:93100.

    15. Sundstrom A, Marklund P, Nilsson L-G, Cruts M,

    Adolfsson R, Van Broeckhoven C, Nyberg L. APOE

    influences on neuropsychological function after mild head

    injury within-person comparisons. Neurology 2004;62:

    19631966.

    16. Azouvi P, Couillet J, Leclercq M, Martin Y, Asloun S,Rousseaux M. Divided attention and mental effort after

    severe traumatic brain injury. Neuropsychologia 2004;42:

    12601268.

    17. Ashman TA, Cantor JB, Gordon WA, Spielman L, Egan M,

    Ginsberg A, Engmann C, Dijkers M, Flanagan S. Objective

    measurement of fatigue following traumatic brain injury.

    Journal of Head Trauma Rehabilitation 2008;23:3340.

    18. Kohl AD, Wylie GR, Genova HM, Hillary FG, Deluca J.

    The neural correlates of cognitive fatigue in traumatic

    brain injury using functional MRI. Brain Injury 2009;23:

    420432.

    19. Dittner AJ, Wessely SC, Brown RG. The assessment of

    fatigue. A practical guide for clinicians and researchers.

    Journal of Psychosomatic Research 2004;56:157170.

    20. Elovic EP, Dobrovic NM, Fellus JL. Fatigue after trau-matic brain injury. In: DeLuca J, editor. Fatigue as a

    window to the brain. Cambridge, MA: MIT Press; 2005.

    pp 89105.

    21. Johansson B, Starmark A, Berglund P, Rodholm M,

    Ronnback L. A self-assessment questionnaire for mental

    fatigue and related symptoms after neurological disorders and

    injuries. Brain Injury; submitted.

    22. Rodholm M, Starmark J-E, Svensson E, Von Essen C.

    Asteno-emotional disorder after aneurysmal SAH: Reliability,

    symptomatology and relation to outcome. Acta Neurologica

    Scandinavica 2001;103:379385.

    23. van Zomeren AH, van den Burg W. Residual complaints

    of patients two years after severe head injury. Journal of

    Neurosurgery and Psychiatry 1985;48:2128.

    24. King NS, Crawford S, Wenden FJ, Moss NEG, Wade DT.The Rivermead post concussion symptoms questionnaire:

    A measure of symptoms commonly experienced after head

    injury and its reliability. Journal of Neurology 1995;24:

    587592.

    25. Svanborg P, Asberg M. A new self-rating scale for depres-

    sion and anxiety states based on the Comprehensive

    Psychopathological Scale. Acta Psychiatrica Scandinavica

    1994;89:2128.

    26. Wilson JTL, Pettigrew LEL, Teasdale GM. Structured

    interviews for the Glasgow Outcome Scale and the

    Extended Glasgow Outcome Scale: Guidelines for their use.

    Journal of Neurotrauma 1998;15:573585.

    27. DeLuca J. Information processing speed: how fast, how

    slow, and how come? In: DeLuca J, Kalmar JH, editors.

    Information processing speed in clinical population.

    New York: Taylor & Francis Group; 2007. pp 265273.

    28. Wechsler D. Wechsler Adult Intelligence Scalethird edition,

    WAIS-III NI. Stockholm: Harcourt Assessment; 2004.

    29. Ellis DC, Kaplan E, Kramer JH. Delis-Kaplan Executive

    Function SystemD-KEFS. San Antonio: Harcourt

    Assessment; 2001.

    30. Reitan RM, Wolfson D. The Halstead-Reitan neuropsycho-

    logical test battery. Theory and clinical interpretation.

    Tucson, AZ: Neuropsychology Press; 1985.

    31. Lezak MD, Howieson DB, Loring DW. Neuropsychological

    assessment. 4th ed. New York: Oxford University Press;

    2004.

    32. Jarpsten B. DLS handledning for skolar 79 och ar 1 i

    gymnasiet. Stockholm: Psykologiforlaget; 2002.

    1036 B. Johansson et al.

  • 8/3/2019 Mental Fatigue and Attention Problems Due to Brain Injury

    11/15

    33. Joy S, Kaplan E, Fein D. Speed and memory in the WAIS-III

    digit symbolcoding subtest across the adult lifespan.

    Archives of Clinical Neuropsychology 2004;19:759767.

    34. Ziino C, Ponsford J. Vigilance and fatigue following

    traumatic brain injury. Journal of the International

    Neuropsychology Society 2006;12:100110.

    35. Tombaugh TN. Trail Making Test A and B: Normative

    data stratified by age and education. Archives of Clinical

    Neuropsychology 2004;19:203214.36. Madigan NK, DeLuca J, Diamond BJ, Tramontano G,

    Averill A. Speed of information processing in traumatic brain

    injury: Modality-specific factors. Journal of Head Trauma

    Rehabilitation 2000;15:943956.

    37. Chiaravalloti ND, Christodoulou C, Demaree HA.

    Differentiating simple versus complex processing speed:

    Influence on new learning and memory performance.

    Journal of Clinical and Experimental Neuropsychology

    2003;25:489501.

    38. DeLuca J, Kalmar JH. Information processing speed in

    clinical population. New York: Taylor & Francis Group;

    2007.

    39. Martin TA, Donders J, Thompson E. Potential of and

    problems with new measures of psychometric intelligence

    after traumatic brain injury. Rehabilitation Psychology2000;45:402408.

    40. Tombaugh TN, Rees L, Stormer P, Harrison AG, Smith A.

    The effect of mild and severe traumatic brain injury on speed

    of information processing as measured by computerized test

    of information processing (CTIP). Archives of Clinical

    Neuropsychology 2007;22:2536.

    41. Wilde N, Strauss E. Functional equivalence of WAIS-III/

    WMS-III digit and spatial span under forward and backward

    recall conditions. Clinical Neuropsychology 2002;16:

    322330.

    42. Kessels RPC, van der Berg E, Brands AMA. The backward

    span of the corsi block-tapping task and its association with

    the WAIS-III digit span. Assessment 2008;15:426434.

    43. DeLuca J, Genova HM, Hillary FG, Wylie G. Neural

    correlates of cognitive fatigue in multiple sclerosis using

    functional MRI. Journal of Neurological Sciences 2008;270:

    2839.

    44. Turner GR, Levine B. Augmented neural activity during

    executive control processing following diffuse axonal injury.Neurology 2008;71:812818.

    45. Park NW, Moscovich M, Robertson IH. Divided attention

    impairments after traumatic brain injury. Neuropsychologia

    1999;37:11191133.

    46. LaCapelle DL, Finlayson MAJ. An evaluation of

    subjective and objective measures of fatigue in patients

    with brain injury and healthy controls. Brain Injury

    1998;12:649659.

    47. Ziino C, Ponsford J. Selective attention deficits and

    subjective fatigue following traumatic brain injury.

    Neuropsychology 2006;20:383390.

    48. Silver JM, Mc Allister JW, Arciniegas DB. Depression and

    cognitive complaints following mild traumatic brain injury.

    American Journal of Psychiatry 2009;166:653661.

    49. van Naalt J, van Zomeren AH, Sluiter WJ, Minderhoud JM.One year outcome in mild to moderate head injury:

    The predictive value of acute injury characteristics related

    to complaints and return to work. Journal of Neurology,

    Neurosurgery and Psychiatry 1999;66:207213.

    50. Draper K, Ponsford J. Cognitive functioning ten years

    following traumatic brain injury and rehabilitation.

    Neuropsychology 2008;22:618625.

    51. Stalnacke B-M. Community integration, social support and

    life satisfaction in relation to symptoms 3 years after mild

    traumatic brain injury. Brain Injury 2007;21:933942.

    Appendix: Adjusted version

    Self report of mental fatigue and related symptoms

    This questionnaire will help us to find out how you perceive your health.

    We are interested in your present condition, that is how you have felt during the past month.

    Each question below is followed by four statements that describe: No (0), Slight (1), Fairly serious (2) and

    Serious (3) problems.

    We would like you to place a circle around the figure before the statement that best describes your problems.

    Should you find that your problem falls between two statements, there are also figures to indicate this.

    1. Fatigue

    Have you felt fatigued during the past month? It does not matter if the fatigue is physical (muscular) or mental.

    If you recently experienced something unusual (for example an accident or short illness) you should try to

    disregard it when assessing your fatigue.0 I do not feel fatigued at all. (No abnormal fatigue, do not need to rest more than usual).

    0.5

    1 I feel fatigued several times every day but I feel more alert after a rest.

    1.5

    2 I feel fatigued for most of the day and taking a rest has little or no effect.

    2.5

    3 I feel fatigued all the time and taking a rest makes no difference.

    2. Lack of initiative

    Do you find it difficult to start things? Do you experience resistance or a lack of initiative when you have to start

    something, no matter whether it is a new task or part of your everyday activities?

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    0 I have no difficulty starting things.

    0.5

    1 I find it more difficult starting things than I used to. Id rather do it some other time.

    1.5

    2 It takes a great effort to start things. This applies to everyday activities such as getting out of bed, washing myself and eating.

    2.5

    3 I cant do the simplest of everyday tasks (eating, getting dressed). I need help with everything.

    3. Mental fatigue

    Does your brain become fatigued quickly when you have to think hard? Do you become mentally fatigued from

    things such as reading, watching TV or taking part in a conversation with several people? Do you have to take

    breaks or change to another activity?

    0 I can manage in the same way as usual. My ability for sustained mental effort is not reduced.

    0.5

    1 I become fatigued quickly but am still able to make the same mental effort as before.

    1.5

    2 I become fatigued quickly and have to take a break or do something else more often than before.

    2.5

    3 I become fatigued so quickly that I can do nothing or have to abandon everything after a short period ($5 minutes).

    4. Mental recoveryIf you have to take a break, how long do you need to recover after you have worked until you drop or are no

    longer able to concentrate on what you are doing?

    0 I need to rest for less than an hour before continuing whatever I am doing.

    0.5

    1 I need to rest for more than an hour but do not require a nights sleep.

    1.5

    2 I need a nights sleep before I can continue whatever I am doing.

    2.5

    3 I need several days rest in order to recover.

    5. Concentration difficulties

    Do you find it difficult to gather your thoughts and concentrate?

    0 I can concentrate as usual.0.5

    1 I sometimes lose concentration, for example when reading or watching TV.

    1.5

    2 I find it so difficult to concentrate that I have problems, for example reading a newspaper or taking part in a conversation with

    a group of people.

    2.5

    3 I always have such difficulty concentrating that it is almost impossible to do anything.

    6. Memory problems

    Do you forget things more often than before, do you need to make notes or do you have to search for things

    at home or at work?

    0 I h ave no memory p roblems.

    0.51 I forget things slightly more often than I should, but I am able to manage by making notes.

    1.5

    2 My poor memory causes frequent problems (for example forgetting important meetings or turning off the cooker).

    2.5

    3 I can hardly remember anything at all.

    7. Slowness of thinking

    Do you feel slow or sluggish when you think about something? Do you feel that it takes an unusually long time

    to conclude a train of thought or solve a task that requires mental effort?

    1038 B. Johansson et al.

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    0 My thoughts are neither slow nor sluggish when it comes to work involving mental effort.

    0.5

    1 My thoughts are a bit slow one or a few times each day when I have to do something that requires serious mental effort.

    1.5

    2 My thoughts often feel slow and sluggish, even when carrying out everyday activities, for example a conversation with a person or

    when reading the newspaper.

    2.5

    3 My thoughts always feel very slow and sluggish.

    8. Sensitivity to stress

    Do you find it difficult to cope with stress, that is doing several things at the same time while under time

    pressure?

    0 I am able to cope with stress in the same way as usual.

    0.5

    1 I become more easily stressed, but only in demanding situations that I was previously able to manage.

    1.5

    2 I become stressed more easily than before. I feel stressed in situations that previously did not bother me.

    2.5

    3 I become stressed very easily. I feel stressed in unfamiliar or trying situations.

    9. Increased tendency to become emotionalDo you find that you cry more easily than previously? Do you often burst into tears when, for example, you

    watch a sad film or talk with your family members? If you recently experienced something unusual (for example

    an accident or short illness) you should try to disregard it in your assessment.

    0 I am not more emotional than I used to be.

    0.5

    1 I am more emotional than other people but it is something that is natural for me. I start to cry or my eyes fill with tears easily,

    but only in relation to things that affect me deeply.

    1.5

    2 My emotions are problematic or embarrassing. I sometimes even start to cry about things that mean nothing to me. I try to avoid

    certain situations because of this.

    2.5

    3 My emotions cause me great problems. They disturb my day-to-day relationship with members of my immediate family and

    make it difficult for me to cope outside the home.

    10. Irritability or a short fuse

    Are you unusually short-tempered or irritable about things that previously did not bother you?

    0 I am not more short-tempered or irritable than I used to be.

    0.5

    1 I become more easily irritated, but it does not last very long.

    1.5

    2 I become irritated very quickly about small things or things that do not bother other people.

    2.5

    3 I react with extreme anger or rage, which I find very difficult to control.

    11. Sensitivity to light

    Are you sensitive to strong light?0 I have no increased sensitivity to light.

    0.5

    1 I sometimes experience problems with strong light such as sunlight reflected by snow, water or glass, or strong lights at home,

    but I am able to cope with it, for example by wearing sunglasses.

    1.5

    2 I am so sensitive to light that I prefer to carry out my daily activities in dim light. I find it difficult to leave the house without

    sunglasses.

    2.5

    3 My sensitivity to light is so strong that I am unable to leave the house without sunglasses. I keep the blinds (or equivalent) drawn

    at all times.

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    12. Sensitivity to noise

    Are you sensitive to noise?

    0 I do not suffer from increased sensitivity to noise.

    0.5

    1 I sometimes have difficulty with loud noise (for example music, noise from the TV or radio or sudden, unexpected sounds),

    but I can deal with it easily by turning down the volume. My sensitivity to noise does not disturb my everyday life.

    1.5

    2 I have a marked over-sensitivity to noise. I have to avoid loud noise or reduce it (for example by means of ear plugs) in order

    to cope with everyday life.

    2.5

    3 My sensitivity to noise is so great that I find it difficult to manage at home, despite sound insulation.

    13. Decreased sleep at night

    Do you sleep badly at night? If you are sleeping more than before at night, please place a circle around the 0.

    If you are taking sleeping tablets and sleep normally, please place a circle around the 0.

    0 I do not sleep less than before.

    0.5

    1 I have slight problems falling asleep or my sleep is shorter, lighter or more restless than before.

    1.5

    2 I sleep at least 2 hours less than before and wake up frequently during the night without anything disturbing me.

    2.53 I sleep less than 23 hours per night.

    14. Increased sleep

    Do you sleep longer and/or more deeply than before? If you are sleeping less than before, please place a circle

    around the 0. NB: Please take account of time spent sleeping during the day.

    0 I do not sleep more than usual

    0.5

    1 I sleep longer or deeper, but less than 2 hours more than usual, including naps during the day.

    1.5

    2 I sleep longer or deeper. At least 2 hours more than usual, including naps.

    2.5

    3 I sleep longer or deeper. At least 4 hours more than usual, and in addition I need to take a nap during the day.

    15. 24-hour variations

    Do you find that at certain times of the day or night the problems we asked about (for example tiredness, lack of

    concentration) are better or worse? In the statements below, regularly means at least 34 days of the week.

    0 I have not noticed that my problems are regularly better or worse at certain times, or I do not have any specific problems.

    1 There is a clear difference between certain times of the day. I can predict that I will feel better at certain times and worse at other

    times.

    2 I feel unwell at all times of the day and night.

    If you experience 24-hour variations:

    When do you feel at your best? Morning Afternoon Evening Night

    When do you feel at your worst? Morning Afternoon Evening Night

    1040 B. Johansson et al.

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