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J Head Trauma Rehabil


Vol. 20, No. 5, pp. 416–425
c 2005 Lippincott Williams & Wilkins, Inc.

Subjective Reports of Fatigue


During Early Recovery From
Traumatic Brain Injury
Susan R. Borgaro, PhD; Jason Baker, PhD;
Jennifer V. Wethe, PhD; George P. Prigatano, PhD;
Christina Kwasnica, MD

Objective: To determine whether patients with traumatic brain injury (TBI) report higher levels
of fatigue than do normal controls and to identify demographic and cognitive correlates of self-
reported fatigue. Design: Prospective study. Setting: Inpatient neurorehabilitation unit in a medi-
cal center and neurological institute. Participants: Forty-seven neurorehabilitation inpatients with
TBI. Main Outcome Measures: Barrow Neurological Institute (BNI) Fatigue Scale and BNI Screen
for Higher Cerebral Functions. Results: Patients reported significantly greater levels of fatigue com-
pared to the levels reported by normal controls, although fatigue was found to be unrelated to
injury severity, number of days from injury to assessment, cognitive impairment, and gender. In-
spection of individual items revealed no significant differences between severe versus moderate
versus mild TBI groups. However, being able to last the day without taking a nap (ie, item 10) was
found to be the most sensitive item associated with fatigue in the TBI group. Conclusions: Re-
sults of this study suggest the need to integrate activities and interventions to increase endurance
in patients with TBI during early rehabilitation. Accommodating regular rest breaks and increasing
restful sleep should be a focus of inpatient neurorehabilitation units. Key words: brain injury,
fatigue, traumatic brain injury

F ATIGUE is a common symptom of many


neurological conditions.1 Although sub-
jective, it is often clinically observed in acute
may have implications for participation in
rehabilitation.20
While there is no universally accepted defi-
and postacute phases of recovery2–14 and in nition of fatigue, most agree that it is a multidi-
patients with unilateral focal and bilateral mensional construct, although variability ex-
lesions.15,16 Physical and cognitive difficul- ists as to its dimensions. For example, Grobar-
ties may be accentuated by fatigue,17 and fa- Murray and colleagues11 described fatigue as
tigue may be exacerbated by involvement in consisting of 3 dimensions: (1) a perceived
physical and cognitive activities. It has been sensation of weariness; (2) a diminished in-
reported in patients with neurologic condi- terest or “task aversion”; and (3) observable
tions, independent of mood disturbances.10 physical signs or somatic symptoms. Smets
It has also been shown to have serious func- and colleagues21 described physical and men-
tional and emotional consequences18,19 and tal components of fatigue as characterized by
the Multidimensional Fatigue Inventory mea-
sured in patients with cancer and chronic fa-
tigue syndrome. The Fatigue Impact Scale2 is
From the Division of Neurology, Barrow designed to measure fatigue as it relates to
Neurological Institute, St Joseph’s Hospital and cognitive, physical, and social functioning in
Medical Center, Phoenix, Ariz.
patients with multiple sclerosis.
Corresponding author: Susan R. Borgaro, PhD, Barrow In traumatic brain injury (TBI), fatigue has
Neurological Institute, St. Joseph’s Hospital and Medical
Center, 350 W Thomas Rd, Phoenix, AZ 85013 (e-mail: been reported as a prominent symptom for
sborgar@chw.edu). both mild and moderate/severe injuries.8,16 It
416
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Fatigue After Traumatic Brain Injury 417

has been documented as the third most preva- scale. Its psychometric properties yielded 5
lent symptom of postconcussive syndrome dimensions when measured on patients with
following headaches and dizziness.22 Other cancer and chronic fatigue. The dimensions
studies have shown similar results.23,24 van were defined as the following: (1) general fa-
Zomeren16 studied reports of 43 symptoms tigue; (2) physical fatigue; (3) reduced activ-
in patients with TBI with a mean duration ity; (4) reduced motivation; and (5) mental
of posttraumatic amnesia of 24.5 days. In the fatigue.
sample studied, fatigue was endorsed as the Although the scales developed to measure
second most common complaint by 41% of fatigue have demonstrated good reliability in
the patients, second only to memory prob- the patient populations studied, most are dis-
lems, which were endorsed by 49% of the ease specific and/or not conducive for assess-
patients. ing fatigue in patients during early rehabilita-
Problems with fatigue have also been tion. For example, the Fatigue Impact Scale
shown to persist during the postacute stages and the Multidimensional Fatigue Inventory
of recovery after TBI. In a study of patients are lengthy and would likely exceed the level
with mild to moderate TBI, 57% of patients of cognitive and mental endurance often dis-
complained of fatigue at 1 month postinjury, played by patients during acute inpatient re-
61% at 3 months postinjury, 45% at 6 months habilitation. The Fatigue Severity Scale, albeit
postinjury, and 45% at 1 year postinjury.25 In shorter in length, and the Multidimensional
a follow-up study of patients with moderate Fatigue Inventory consist of items that are not
to severe TBI, 68% complained of fatigue at necessarily relevant or specific enough to the
2 years postinjury, while 73% complained of experiences of patients on an acute neurore-
fatigue at 5 years postinjury.26 habilitation setting.
There are few published questionnaires The present study introduces a new mea-
that are specifically designed to quantify fa- sure of self-reported fatigue—the Barrow Neu-
tigue, particularly during the acute stages of rological Institute Fatigue Scale (BNI Fatigue
recovery after brain injury. Typically, an as- Scale).28 The BNI Fatigue Scale was specifi-
sessment of fatigue is obtained via a detailed cally developed to provide a quick quantifi-
history,27 a structured interview,2 or question- able self-report assessment of fatigue in pa-
naires designed to measure broader condi- tients during early rehabilitation from brain
tions (eg, Beck Depression Inventory). The injury. It is brief in length and easy to under-
most recognized published questionnaires stand, making it unique and conducive for ad-
were developed to assess fatigue in patients ministration on an acute inpatient neuroreha-
with multiple sclerosis. The Fatigue Impact bilitation unit. Whether the scale is sensitive
Scale,2 for example, is a 40-item self-report for detecting self-reports of fatigue in pa-
questionnaire that asks about the role of fa- tients after TBI remains to be empirically de-
tigue as it relates to cognitive, physical, and so- termined and is a focus of this exploratory
cial functioning in patients with multiple scle- study.
rosis. Responses are rated on a scale of 0 (no The purpose of the present research is 2-
problem) to 4 (extreme problem). The Fatigue fold. First, this study will examine self-reports
Severity Scale12 is a 9-item self-report ques- of fatigue in patients with TBI during early
tionnaire that asks patients to rate on a scale rehabilitation using the BNI Fatigue Scale. It
from 1 (strongly disagree) to 7 (strongly agree) is expected that the patients with TBI will
the degree to which fatigue interferes with report significantly higher levels of fatigue
their functioning. The Fatigue Severity Scale compared to the levels reported by a sam-
has demonstrated sensitivity to the fatigue ple of normal controls. A second focus of this
problems of patients with multiple sclero- study is to determine whether there is an asso-
sis. The Multidimensional Fatigue Inventory21 ciation between self-reported fatigue and po-
consists of 24 items that are rated on a 7-point tential moderating variables. The number of
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418 JOURNAL OF HEAD TRAUMA REHABILITATION/SEPTEMBER–OCTOBER 2005

days that pass from injury to neuropsycho- of 8 or less), 18 patients had sustained mod-
logical assessment has been positively corre- erate head injuries (GCS score between 9
lated with severity of injury.29–31 Whether in- and 12), and 11 patients had sustained mild
jury severity, number of days postinjury, and head injuries (GCS scores in the 13–15 range).
cognitive impairment are associated with self- Of the 11 patients with mild injuries, 4
reported fatigue has not yet been studied (36%) had injuries complicated by intracra-
with the BNI Fatigue Scale. Also, fatigue has nial lesions as visualized by computed tomog-
been shown to differ for gender across several raphy and/or magnetic resonance imaging,
studies11,32 and will therefore be examined in whereas 7 (64%) had uncomplicated injuries.
the present study. Of the total 40 patients with visualized in-
juries, 50% had bilateral lesions, 17.5% had left
hemisphere lesions, and 22.5% had right
METHODS hemisphere lesions. Another 10% had visu-
alized lesions in the brain stem, cerebel-
Participants lum, or an unspecified location. The most
Fatigue was studied in 47 patients with common visualized lesions were contusions
TBIs, admitted to the inpatient neurorehabil- (45%), hemorrhages (39%), and hematomas
itation unit of the BNI in Phoenix, Ariz. Pa- (16%).
tients had varying levels of injury severity as The control group was a convenience sam-
classified by admission Glasgow Come Scale ple of 30 volunteers recruited from the gen-
(GCS) score.33 Average age was 35.93 (SD = eral population. Participants were included
16.49), and average education was 12.43 if they reported no history of psychiatric or
(SD = 2.33) years. Table 1 shows the demo- neurologic disease. Mean age was 36.20 years
graphic and neurologic features of the patient (SD = 19.46), and mean education was 13.46
group. years (SD = 1.67). Sixty-two percent of
Eighteen patients had sustained severe the normal control participants were male
head injuries (as evidenced by a GCS score (Table 1).

Table 1. Demographic and neurologic characteristics of patient and control groups

Patients with
traumatic brain Controls
injury (n = 45) (n = 30)
M SD M SD P
Age 35.93 16.49 36.20 19.46 .951
Education 12.43 2.33 13.46 1.67 .071
Gender
% Male 55.10 62.5 .238
Glasgow Coma Scale score 9.39 4.11
Postinjury days 24.37 17.01
Range of days 3–81
Lesion location, %
Right 22.5
Left 17.5
Bilateral 40.0
Other 10.0
Barrow Neurological Institute T Score 18.44 17.81
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Fatigue After Traumatic Brain Injury 419

Independent t tests were conducted to de- ness versus Performance. For a detailed
termine whether the groups differed on age description of the individual items, see
and education. Chi-square analysis was con- Prigatano et al.34 A total raw score provides
ducted to determine whether there were any an overall index of cognitive functioning. It
gender differences between the groups. The is obtained by summing all of the subtest
analyses showed no statistical differences be- raw scores. Higher scores indicate a higher
tween the groups on age (t73 = 0.229, P = level of functioning. The total raw score may
.819), education (t73 = 1.90, P = .071), or gen- be converted to an age-corrected standard
der (X2 = −0.143, P = .238). (T) score using the norms of Prigatano and
colleagues.34 The total BNIS T score was used
Measures as a dependent variable of overall cognitive
BNI Fatigue Scale functioning.

The BNI Fatigue Scale28 (Appendix) con- Procedures


sists of 10 items that are rated on a 7-point
scale. The scale ranges from 0 to 1 (rarely a All patients who met the inclusion criteria
problem), 2 to 3 (occasional problem, but not were evaluated within the first 90 days of their
frequent), 4 to 5 (frequent problem), and 6 injury. Participants were interviewed and ad-
to 7 (a problem most of the time). Patients ministered the BNI Fatigue Scale and the BNIS
are asked to characterize their level of fatigue by either a staff clinical neuropsychologist or
since their injury by choosing a number that a postdoctoral resident in clinical neuropsy-
best describes their response. A total score is chology, as part of their neuropsychological
obtained on items 1 through 10. A final item examination.
(item 11) asks patients to circle their overall
level of fatigue since their injury on a scale RESULTS
from 0 (no problem) to 10 (severe problem).
Patients with acute TBI typically complete the Performances on BNI Fatigue Scale
questionnaire within 5 minutes. The scale was It was expected that the TBI group as a
found to have good test-retest reliability on a whole would report higher levels of fatigue
heterogeneous sample (n = 30) of inpatient than would the normal control group. Using
neurologic patients (r = 0.96). Additional re- independent t tests and Bonferroni statistics,
liability and psychometric properties of this with alpha set at P less than .004 for multi-
scale have been documented elsewhere (see ple comparisons, it was found that the TBI
Borgaro et al28 ). group reported higher levels of fatigue on the
BNI Fatigue Scale. Inspection of specific items
BNI Screen for Higher Cerebral showed significantly higher reports of fatigue
Functions in the TBI group on items 4 (How difficult is
The BNI Screen for Higher Cerebral Func- it for me to complete a task without becom-
tions (BNIS)34,35 was designed to provide a ing tired?), 5 (How difficult is it for me to stay
brief but valid assessment of higher cerebral alert during activities?), 7 (How difficult is it
functions from acute to chronic stages of for me to stay out of my bed during the day?),
various brain disorders. Initial studies have 10 (How difficult is it for me to last the day
demonstrated its reliability and validity.36 The without taking a nap?), and 11 (overall index
BNIS takes approximately 10 to 25 minutes to of fatigue) (Table 2).
administer. It is composed of the following 7 A stepwise multiple regression analysis
subtests: (1) Speech and Language; (2) Orien- was performed to determine whether any of
tation; (3) Attention/Concentration; (4) Visu- the statistically significant items listed above
ospatial and Visual Problem Solving; (5) Learn- (ie, items 4, 5, 7, 10, and 11) would be most
ing and Memory; (6) Affect; and (7) Aware- associated with the TBI group. The single item
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420 JOURNAL OF HEAD TRAUMA REHABILITATION/SEPTEMBER–OCTOBER 2005

Table 2. Group differences on Barrow Neurological Institute Fatigue Scale items

Patients with
traumatic brain Controls
injury (n = 47) (n = 30)
M SD M SD t P
Item 1 2.44 1.71 1.87 1.91 −1.26 .212
Item 2 2.13 1.98 1.17 1.13 −2.58 .012
Item 3 1.89 2.05 1.00 1.41 −2.12 .038
Item 4 2.18 1.97 0.83 0.76 −4.05 .000∗
Item 5 1.84 1.99 0.62 0.57 −3.82 .000∗
Item 6 1.60 1.90 1.54 1.93 −0.12 .904
Item 7 2.36 2.21 0.79 0.83 −4.20 .000∗
Item 8 2.04 2.08 1.95 1.42 −0.20 .840
Item 9 1.73 1.92 0.95 0.99 −2.20 .031
Item 10 2.53 2.23 0.66 0.76 −5.08 .000∗
Total score 20.71 16.49 11.41 6.99 −3.27 .002∗
Overall fatigue index 4.44 3.09 2.50 1.93 −3.20 .002∗

∗ Significant after appropriate adjustment of alpha level (α = .004).

most associated with TBI was item 10 (How injury to assessment (F2,45 = 4.18, P = .022).
difficult is it for me to last the day without tak- There also was a dose-response relationship
ing a nap?) (r2 = 0.183, F = 15.49, P = .000). between TBI groups and total cognitive im-
pairment score on the BNIS (F2,45 = 6.45,
Correlates of fatigue in TBI P = .004), with patients with severe TBI hav-
To better understand the role of self- ing the greatest cognitive impairment (M =
reported fatigue in the TBI group, poten- 13.22, SD = 14.70), followed by the moder-
tial moderating variables were examined for ate (M = 16.56, SD = 18.47) and mild groups
their effects on fatigue. Pearson correlations (M = 36.00, SD = 13.25), respectively. With
yielded no statistically significant findings for days postinjury and BNIS score covaried, and
cognitive performance on the BNIS (r = alpha set at P less than .004 for multiple com-
−0.08, P = .628), days postinjury (r = −0.12, parisons using Bonferroni statistics, analyses
P = .424), or injury severity as per the GCS of covariance revealed no significant differ-
score at admission (r = −.05, P = .738). An ences between the TBI groups on any of the
independent t test revealed no significant dif- BNI Fatigue Scale items.
ference between gender and self-reported fa-
tigue (t73 = −1.01, P = .317). DISCUSSION

Injury severity and fatigue This study examined self-reports of fatigue


Individual fatigue items were examined for in patients with TBI during early rehabilita-
differences between TBI groups (mild vs mod- tion. Self-reported fatigue was found to be a
erate vs severe) as classified by GCS score problem during the early stages of recovery
(Table 3). The groups did not differ on age from TBI, as measured by the BNI Fatigue
(F2,45 = 2.65, P = .079), education (F2,45 = Scale. Patients with TBI reported significantly
.029, P = .971), or gender (X2 = 0.418, P = greater fatigue than did normal controls, al-
.811). The TBI groups did differ on days from though it was found to be unrelated to injury
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Fatigue After Traumatic Brain Injury 421

Table 3. Performance across traumatic brain injury groups on the Barrow Neurological Institute
Fatigue Scale total score∗

Severe (n = 18) Moderate (n = 18) Mild (n = 11) F P


Item 1 2.17 (1.62) 2.44 (1.85) 2.91 (1.51) 0.55 .653
Item 2 2.44 (2.17) 1.67 (1.41) 2.36 (2.29) 0.79 .506
Item 3 2.50 (1.98) 1.55 (2.12) 1.36 (1.74) 1.43 .249
Item 4 1.88 (2.05) 2.00 (1.85) 2.64 (2.01) 1.30 .288
Item 5 1.83 (1.98) 1.61 (1.94) 1.91 (2.21) 0.43 .730
Item 6 1.22 (1.44) 1.89 (2.05) 1.82 (2.22) 0.34 .796
Item 7 2.89 (2.72) 1.61 (1.68) 2.60 (1.58) 1.43 .247
Item 8 2.56 (2.45) 1.61 (1.58) 2.09 (1.87) 0.83 .482
Item 9 1.61 (2.00) 1.67 (1.78) 2.09 (1.92) 0.44 .728
Item 10 2.61 (2.61) 2.22 (2.02) 2.91 (1.75) 0.93 .433
Total (1–10) 21.72 (16.93) 18.28 (15.97) 22.45 (16.14) 0.55 .650
Overall index 4.44 (3.32) 4.17 (3.22) 5.09 (2.38) 0.46 .036

∗ Values are mean (SD).

severity, number of days postinjury, cogni- suggesting that fatigue may be secondary to
tive impairment score on the BNIS, and gen- sleep disturbances for some patients. Not all
der. No differences were found between TBI patients with fatigue however reported sleep
groups on the BNI Fatigue Scale when classi- disturbances, suggesting that fatigue may be a
fied by injury severity (ie, mild, moderate, and separate domain. Thus, fatigue after brain in-
severe). jury may be due in part to both sleep depriva-
Inspection of patient scores revealed great- tion and brain injury. Item 10 may be a sensi-
est difficulty on items related to staying alert tive and useful quantifiable measure of fatigue
during rehabilitation activities, completing after TBI, regardless of sleep patterns.
tasks without becoming tired, and staying Injury severity and cognitive impairment
awake and out of bed during the day. Being on the BNIS were unrelated to fatigue as mea-
able to last the day without taking a nap (item sured by the BNI Fatigue Scale. The lack of re-
10) was found to be the most sensitive item as- lationship may be due to the acute nature of
sociated with TBI. The sensitivity of this item patients studied. Patients may be too severely
may be due in part to sleep disturbances after injured, hence requiring inpatient rehabilita-
TBI. Sleep disturbances have been frequently tion, to show differences in fatigue. It is pos-
reported in patients after TBI37,38 and partic- sible that specific patterns of self-reported fa-
ularly during early rehabilitation because of a tigue might emerge as patients progress from
variety of factors, including scheduled thera- acute to postacute stages of recovery. Fur-
pies, recreational activities, visitors, medical/ thermore, the severe TBI group in this study
nursing procedures, noise/activity level, etc. was limited to those who were able to com-
Although sleep disturbances may be com- plete a brief assessment. Thus, the most se-
mon during early recovery, fatigue may be re- vere patients (ie, those who could not com-
lated but independent of sleep for some pa- plete a brief assessment) were excluded from
tients. For example, Clinchot and colleagues39 this study.
found that 50% of the 45 patients studied by Other studies have reported no relationship
them reported sleep disturbances, while 63% between fatigue and cognitive impairment.
reported fatigue. Of the 50% of patients with For example, recent research by Parmenter
sleep disturbances, 80% also reported fatigue, and colleagues40 showed no differences
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422 JOURNAL OF HEAD TRAUMA REHABILITATION/SEPTEMBER–OCTOBER 2005

in cognitive performance in patients with important factors during early inpatient neu-
multiple sclerosis when tested during pe- rorehabilitation.
riods of high versus low fatigue. Similarly, Results of this study emphasize how self-
ratings of fatigue were unrelated to cogni- reported fatigue is perceived as a problem
tive performance in patients with chronic fa- after TBI regardless of injury severity, and
tigue syndrome.41 Other studies, however, may have implications for early rehabilitation.
have shown an association between fatigue Patients are expected to complete physical,
and cognitive performance in patients with occupational, and speech therapies on inpa-
myasthenia gravis42,43 and chronic fatigue tient rehabilitation units. Each therapy typi-
syndrome.32 cally takes 1 hour, but is often done in half-
The present study found no differences be- hour sessions. Thus, much of the patient’s
tween fatigue and gender after TBI, which time during the day is occupied by therapies
may be characteristic of the acute and dif- and other activities, with little time for rest.
fuse nature of TBI. However, several studies When they are done with therapies, they are
have documented differences between fa- often visited by family members and friends.
tigue and gender, with females often report- In addition, it is often difficult to obtain a
ing more fatigue than do males. This pattern restful night’s sleep because of the nature of
has been reported in patients with myasthenia an inpatient unit, often leaving the patient fa-
gravis,11 sleep apnea,44 major depression,45 tigued the next morning. Scheduling regular
chronic fatigue syndrome,46 chronic hepati- rest breaks during the day may help to reduce
tis C,47 heart disease,48–50 cancer,51,52 and a patient’s fatigue and should be considered
rheumatoid arthritis.53 It is unknown why fe- on inpatient rehabilitation units. Also, activi-
males have shown higher rates of fatigue com- ties aimed at helping to increase endurance
pared to those shown by males across the dif- (eg, mild exercise) would likely facilitate the
ferent conditions noted above. reduction of fatigue and should be considered
This study consisted of several limitations as a focus of early remediation interventions.
that should be considered when interpreting It is not uncommon for patients with TBI
the present results. Medication and related is- to request frequent breaks or end a cognitive
sues (eg, dosage, type) were not controlled task prematurely when they cannot sustain
for, which may have impacted self-reported fa- the mental energy or “drive”54 required to per-
tigue levels. Furthermore, this study did not form a task. Future research should be aimed
include a general medical control group to ex- at identifying potential correlates of sustained
amine potential hospital-related variables im- intensity or energy. Halstead,55 for example,
pacting fatigue (eg, medical conditions, com- referred to the “cerebral power” factor or en-
plications). Finally, future studies using the ergy source in describing tests of intellectual
BNI Fatigue Scale should examine the impact energy. Identifying cognitive tests sensitive to
of other variables on fatigue, including sleep fatigue would allow for measurement of clini-
deprivation and injury location, as these are cal intervention and outcome.

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Fatigue After Traumatic Brain Injury 425

Appendix

Please rate the extent to which each of the items below has been a problem for you since
your injury. You should chose only ONE number from 0 to 7 on the scale below when making
your response.

0 1 2 3 4 5 6 7
Rarely a problem Occasional problem, A frequent problem A problem most
but not frequent of the time

1. How difficult is it for me to maintain my energy throughout the day?


2. How difficult is it for me to participate in activities because of fatigue?
3. How difficult is it for me to stay awake during the day?
4. How difficult is it for me to complete a task without becoming tired?
5. How difficult is it for me to stay alert during activities?
6. How difficult is it for me to build my energy level once I wake up in the morning?
7. How difficult is it for me to stay out of my bed during the day?
8. How difficult is it for me to stay alert when I am not involved in something?
9. How difficult is it for me to attend to something without becoming sleepy?
10. How difficult is it for me to last the day without taking a nap?
TOTAL RAW SCORE = T SCORE =

11. Please circle your OVERALL level of fatigue since your injury:

0 1 2 3 4 5 6 7 8 9 10
No problem Severe Problem

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