Asian Journal of Psychiatry 26 (2017) 1–5

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Asian Journal of Psychiatry

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

Factors associated with multidimensional aspect of post-stroke fatigue

in acute stroke period
Hitoshi Mutaia,b , Tomomi Furukawaa , Ayumi Houria , Akihito Suzukia , Tokiji Haniharab,c,*
a
Department of Rehabilitation, Azumino Red Cross Hospital, 5685 Toyoshina, Azumino, Nagano 399-8292, Japan
b
School of Health Sciences, Shinshu University School of Medicine, 3-1-1 Asahi, Matsumoto, Nagano 390-8621, Japan
c
Nagano Prefectural Mental Wellness Center Komagane, 2901 Shimodaira, Komagane, Nagano 399-4101, Japan

A R T I C L E I N F O A B S T R A C T

Article history: Background: Post-stroke fatigue (PSF) is a frequent and distressing consequence of stroke, and can be both
Received 19 April 2016 acute and long lasting. We aimed to investigate multidimensional aspects of acute PSF and to determine
Received in revised form 14 December 2016 the clinical factors relevant to acute PSF.
Accepted 27 December 2016
Methods: We collected data of 101 patients admitted to the hospital for acute stroke. PSF was assessed
Available online xxx
using the Multidimensional Fatigue Inventory within 2 weeks of stroke. Measures included Mini-Mental
State Examination, Hospital Anxiety and Depression Scale, and Functional Independence Measure. Stroke
Keywords:
character, lesion location, and clinical variables that potentially influence PSF were also collected.
Post-stroke fatigue
Stroke
Results: The prevalence of pathological fatigue is 56.4% within 2 weeks of stroke. Binary logistic
Anxiety regression analysis revealed that anxiety was the only predictor for presence of PSF (OR = 1.32, 95% CI:
Depression 1.13–1.53, P < 0.001). Multivariate stepwise regression analysis showed anxiety, right lesion side,
thalamus, and/or brainstem were independently associated with general fatigue, right lesion side,
depression, diabetes mellitus, and anxiety with physical fatigue, depression with reduced activity,
depression, and BMI with reduced motivation, depression, and diabetes mellitus with mental fatigue.
Conclusions: PSF was highly prevalent in the acute phase, and specific factors including lesion location
(right side lesion, thalamic and brainstem lesion), anxiety, and depression were independently associated
with multidimensional aspects of PSF. Further study is needed to elucidate how specific structural lesions
and anxiety symptoms relate to the development of early fatigue following stroke.
© 2016 Elsevier B.V. All rights reserved.

1. Introduction relieved by rest (Chaudhuri and Behan, 2004; Wu et al., 2015).

Post-stroke fatigue (PSF) is one of the most prevalent and
distressing symptoms of stroke, with 23–75% prevalence (Ingles
et al., 1999; Staub and Bogousslavsky, 2001; Choi-Kwon and Kim,
2011). It may substantially persist after stroke and negatively
impact rehabilitation, functioning, and quality of life (van der Werf
et al., 2001; Snaphaan et al., 2011; Radman et al., 2012). Fatigue is a
complex, multifaceted, and entirely subjective construct. PSF
differs from normal fatigue resulting from overexertion and is not
Abbreviations: PSF, post-stroke fatigue; MFI, multidimensional fatigue invento-
ry; SIAS, stroke impairment assessment set; MMSE, mini-mental state examination;
HADS, hospital anxiety and depression scale; HADS-A, hospital anxiety and
depression scale anxiety subscale; HADS-D, hospital anxiety and depression scale
depression subscale; FIM, functional independence measurement; BMI, body mass
index.
* Corresponding author at: Nagano Prefectural Mental Wellness Center,
Komagane, Japan.
E-mail address: qhaniha@shinshu-u.ac.jp (T. Hanihara).
Despite its prevalence, little is known about the underlying
mechanism and related factors. Many studies have demonstrated a
robust relationship between PSF and post-stroke depression (van
der Werf et al., 2001; Lerdal et al., 2011). However, PSF can also
occur in the absence of depression (van der Werf et al., 2001), and
that post-stroke depression and PSF are dissociated from each
other. In addition to post-stroke depression, post-stroke anxiety is
also important neuropsychiatric consequences of stroke, and has
been recently investigated (Campbell Burton et al., 2013). The
association between PSF and post-stroke anxiety has been
controversial (Wu et al., 2014).
Considering PSF etiology, both the direct consequence of
neurologic insult and psychosocial factors are thought to be
involved. The stroke itself may be more influential in the early
period, while psychosocial factors become more dominant in the
chronic phase. A recent study (Lerdal and Gay, 2013) reported that
acute phase fatigue is a significant predictor of later fatigue.
However, studies investigating PSF in the acute phase, such as the
first or second week following stroke, are scarce (Chaudhuri and

http://dx.doi.org/10.1016/j.ajp.2016.12.015
1876-2018/© 2016 Elsevier B.V. All rights reserved.
2 H. Mutai et al. / Asian Journal of PsychiatryAJP 26 (2017) 1–5
Behan, 2004; Schepers et al., 2006; Christensen et al., 2008).
Because the acute phase may represent a critical period for
functional recovery, it is important to clarify the prevalence,
characteristics, and possible contributing factors of PSF.
This study thus investigated the prevalence and characteristics
of PSF among stroke patients admitted on the acute ward using
multidimensional fatigue inventory and determined the relation-
ship between clinical variables including affective symptoms and
PSF.
2. Methods
2.1. Subject
One hundred one patients with acute stroke participated in the
study, recruited from 220 consecutive stroke patients admitted to
the acute ward of Azumino Red Cross Hospital between October
2012 and November 2013. Inclusion criteria were ischemic or
hemorrhagic stroke diagnosed by clinical and radiographic
findings. Severe confusion, severe aphasia, or severe motor
complications with immobility that could impede active rehabili-
tation were not excluded. A cross-sectional, descriptive analysis
design was developed. All interviews and assessments were
conducted within 2 weeks after stroke and were administered by
the authors (H. M, T. F, A. H and A. S: certified occupational
therapists trained for this study). The Ethical Review Board of
Azumino Red Cross Hospital and the Ethical Committee of Shinshu
University approved this study. Participating patients or their
relatives gave informed consent.
2.2. Assessment of fatigue
To characterize PSF, we employed Multidimensional Fatigue
Inventory (MFI) as the main outcome measure (Smets et al., 1995;
Sugaya et al., 2005). The MFI is a self-report questionnaire that
assesses the impact of fatigue and comprises five dimensions:
general fatigue, physical fatigue, reduced activity, reduced
motivation, and mental fatigue. General fatigue measures overall
feelings of tiredness, physical fatigue measures physical sensations
related to feelings of tiredness, reduced activity measures amounts
of daily activities, reduced motivation measures motivation level in
daily activities, and mental fatigue includes deficits in cognitive
functioning. MFI scoring ranges for each factor are 4–20, with
higher scores indicating stronger fatigue.
2.3. Clinical characteristics
The following clinical information were collected: body mass
index, medical complications (hypertension, myocardial infarc-
tion, angina, atrial fibrillation, arrhythmia, cardiac failure, and
diabetes mellitus), stroke event (first or recurrent), and ischemic or
hemorrhagic stroke.
Lesion side (right or left) and location were recorded with MRI
or CT upon admission. The following lesion locations were used:
frontal, temporal, occipital, parietal, basal ganglia, internal capsule,
thalamic, brainstem, and cerebellar, divided into four groups
according to their lesion location: cortical, thalamic and brainstem,
basal ganglia and internal capsule, or cerebellar (Radman et al.,
2012). In cases with multiple lesions, all of them were counted.
Impairment associated with stroke was assessed using Stroke
Impairment Assessment Set (SIAS) (Chino et al., 1994). SIAS
consists of nine functions: motor paralysis, muscle tone, sensory
disturbance, range of motion, pain, trunk function, visuospatial
perception, aphasia, and non-paretic limb function. Activities in
daily living (ADL) were assessed using Functional Independence
Measure (FIM) (Granger et al., 1993). FIM consists of motor and
cognitive FIM. Thirteen items comprise motor FIM and five items
comprise cognitive FIM. The scoring ranges of FIM are 18–126, with
higher scores indicating higher ADL level. SIAS and FIM were
administered by the authors within one week at admission. Global
cognition was assessed by Mini-Mental State Examination (MMSE)
(Folstein et al., 1975). Depression and anxiety symptoms were
assessed by Hospital Anxiety and Depression Scale (HADS) (Sagen
et al., 2010). HADS is a self-report questionnaire for psychological
distress, including the HADS Anxiety subscale (HADS-A) and the
HADS Depression subscale (HADS-D), each of which have seven
items with responses ranging from 0 to 3. Scoring ranges of each
scale are 0–21; higher scores indicate increased symptoms. The
MFI, MMSE and HADS were performed during the second week of
stroke.
2.4. Statistical analysis
All statistical analyses were performed with SPSS for Windows
22.0 (IBM, Chicago, USA). Correlations between parameters were
computed using Spearman’s correlation analysis. Cross-sectional
predictive factors for PSF were determined by binary logistic
regression analyses. Independent variables included age, sex,
stroke event, stroke type, lesion side, lesion locations, medical
complications, body mass index, FIM, MMSE, HADS-D, and HADS-
A. We also collected SIAS motor paralysis and pain scores, because
both severity of paralysis and pain were known to be possibly
associated with PFS (Naess et al., 2010; Lerdal et al., 2011). For
binary logistic regression models, lesion locations were bisected
into two categories (e.g. thalamus or brainstem/other) and
repeatedly analyzed by each four group.
Predictive factors of MFI in each dimension were determined by
multivariate stepwise regression analyses. Independent variables
were the same as in binary logistic regression analyses. In all
analyses, a p-value <0.05 was considered statistically significant.
In regression models, the variance inflation factor was also
estimated to detect multicollinearity among predictors.
3. Results
3.1. Demographic information
Socio-demographic characteristics, cognitive status, medical
complications, and SIAS scores are presented in Table 1. The mean
age of the subjects was 74.4  11.6 years, and 33.7% were female.
Records of onset indicated that 73.3% were admitted with their
first episode of stroke, and 75.2% of subjects suffered ischemic
stroke. Lesion distribution was 46.5% right, 39.6% left, and 3.0%
bilateral. Lesion locations were 58 cortical, 9 thalamic, 26 basal
ganglia and internal capsule, 11 cerebellum, and 9 brainstem.
Twelve patients had combination lesions; 7 cortical + basal
ganglia and internal capsule, 2 cortical + cerebellum, 2 thalamus +
basal ganglia and internal capsule and 1 cerebellum + brainstem.
Mean MMSE score was 22.2  7.8. SIAS at the time of admission
indicated that 24.8% had severe motor paralysis and 15.8% had
pain.
3.2. Fatigue, mood, and functional assessments
The means, standard deviations, and prevalence of pathological
fatigue on MFI are presented in Table 2. With reference to cut-off
values used in the literatures, we employed a general fatigue score
12 as clinically significant for pathological fatigue (Choi-Kwon
et al., 2005; Christensen et al., 2008). The prevalence of
pathological fatigue was 56.4%. Spearman’s correlation was
calculated for each MFI dimension to examine intercorrelation.
MFI general fatigue and physical fatigue were moderately
 H. Mutai et al. / Asian Journal of PsychiatryAJP 26 (2017) 1–5 3

Table 1
Clinical characteristics of patients at admission.

Characteristics (n = 101)
Age Mean age  SD 74.4  11.6
Sex Male/female 67/34
Stroke event First/recurrent 74/25
Stroke type Infarction/hemorrhage 78/23
Lesion side Right/left/both/unidentified 47/40/3/11
Lesion location Cortical/thalamus/basal ganglia and internal capsule/cerebellum/brainstem 58/9/26/11/9
Combined lesions 12
MMSE Mean  SD 22.2  7.8
SIAS
Motor paralysis Normal/slight/moderate/severe 36/24/16/25
Muscle tone Normal/hypertonia/hypotonia 65/20/16
Sensory disturbance Normal/slight/moderate/severe 42/34/11/14
Range of motion Normal/restriction 95/6
Pain No/yes 85/16
Trunk function Normal/decline 42/59
Visuospatial perception Normal/decline 62/39
Aphasia Normal/slight 86/15
Non-paretic limbs function Normal/dysfunction 50/51
Body mass index Mean  SD 22.8  3.5

MMSE, Mini Mental State; SIAS, Stroke Impairment Assessment Set.

correlated (r = 0.55, p < 0.001), while general fatigue and mental or anxiety (b = 0.33, p = 0.001; b = 0.33, P = 0.002; b = 0.24,
fatigue were weakly correlated (r = 0.32, p < 0.001). p = 0.018; and b = 0.24, p = 0.019, respectively); reduced activity 
The results of correlational analysis between MFI and FIM, depression (b = 0.40, p = 0.001); reduced motivation  depression
MMSE, and HADS are presented in Table 3. Depression was or BMI (b = 0.56, p < 0.001; b = 0.25, p = 0.016, respectively); and
significantly correlated with all MFI dimensions, but correlations mental fatigue  depression or diabetes mellitus (b = 0.52,
between depression and general (r = 0.21, p < 0.05) or physical p < 0.001; b = 0.30, p = 0.004; Table 4). The variance inflation
fatigue (r = 0.28, p < 0.01) were weaker than other dimensions. factor was within an acceptable range in the final models.
Anxiety was significantly correlated with general (r = 0.47, p < 0.01)
and physical fatigue (r = 0.32, p < 0.01). The total FIM score are only 4. Discussion
correlated with reduced activity (r = 0.25, p < 0.05). There was no
significant correlation between MMSE and all MFI dimensions In this study, PSF was highly prevalent in the acute phase in
(Table 3). stroke inpatients, in 56% of our sample. All MFI subscales were
higher than normal elderly values (Sugaya et al., 2005) or stroke
3.3. Factors associated with multidimensional aspects of PSF patients in previous studies (Christensen et al., 2008). Anxiety
symptoms were best correlated with general and physical fatigue,
Variables associated with the presence of pathological fatigue while depressive symptoms were best correlated with reduced
(general fatigue score 12) were determined by binary logistic activity, reduced motivation, and mental fatigue. Binary logistical
regression analysis. Anxiety (OR = 1.32, 95% CI: 1.13–1.53, regression analyses confirmed anxiety score was the only predictor
p < 0.001) was significantly associated with PSF presence. for the presence of pathological fatigue. Multivariate stepwise
Variables associated with the each MFI dimension on multivar- regression analysis suggested that anxiety score, right side lesions,
iate stepwise regression analyses were as follows: general fatigue and thalamic or brainstem lesions were independent predictors of
 anxiety, right side lesion, or thalamus and/or brainstem (b = 0.51, general fatigue.
p < 0.001; b = 0.34, p < 0.001; and b = 0.23, p = 0.016, respectively); A number of longitudinal cohort studies reported time courses
physical fatigue  right side lesion, depression, diabetes mellitus, of PSF for individual patients, showing that PSF is relatively stable
in patients after a stroke, likely to persist over time (van der Werf
et al., 2001; Snaphaan et al., 2011; Radman et al., 2012). However,
Table 2
Fatigue, mood, and functional assessments. studies investigating the prevalence of PSF in the acute phase are
scarce. Schepers et al. (2006) reported 51% of patients had severe
Assessment
fatigue indicated by Fatigue Severity Scales at admission, and
MFI Mean  SD 11.7  3.6 Christensen et al. (2008) reported that 59% of patients had
General fatigue 13.0  3.7
pathological fatigue 10 days after stroke. This study also indicated
Physical fatigue 12.6  3.8
Reduced activity 10.0  3.6 that PSF was highly prevalent in the acute phase.
Reduced motivation 12.0  3.6 We found moderate correlation between general and physical
Mental fatigue fatigue on the MFI. Previous studies investigating MFI’s structural
Post stroke fatigue (PSF) No/yes 44/57 validity in patients with cancer (Smets et al., 1995) and Parkinson’s
(General fatigue score 12) % 56.4
Prevalence of PSF
disease (Elbers et al., 2012), using principal component analysis,
FIM Mean  SD 72.8  28.9 suggested that the four-factor model, combining most general and
Total 46.5  23.7 physical fatigue dimensions in one factor, might be appropriate.
Motor 26.3  7.4 We used MFI as the main outcome measure to characterize PSF
Cognitive
among acute stroke patients because we were especially interested
HADS Mean  SD 7.4  4.3 (24.7%)
Anxiety Score 11 (%) 7.8  3.9 (26.8%) in temporal relationships between PSF and affective symptoms.
Depression Depression was significantly related to each of the five fatigue
MFI, Multidimensional Fatigue Inventory; FIM, Functional Independence Measure;
dimensions; 27% of our sample had severe depressive symptoms
HADS, Hospital Anxiety and Depression Scale. (11 HADS-D score). The estimated prevalence of post-stroke
4 H. Mutai et al. / Asian Journal of PsychiatryAJP 26 (2017) 1–5

Table 3
Spearman’s correlation between MFI and FIM, MMSE, and HADS (Anxiety and Depression).

General fatigue Physical fatigue Reduced activity Reduced motivation Mental fatigue
FIM 0.15 0.15 0.25* 0.16 0.15
MMSE 0.07 0.09 0.17 0.19 0.12
Anxiety 0.47** 0.32** 0.13 0.12 0.13
Depression 0.21* 0.28** 0.40** 0.44** 0.46**

Spearman’s rank correlation coefficient. MFI, Multidimensional Fatigue Inventory; FIM, functional independence measure; MMSE, mini mental state examination, HADS,
Hospital Anxiety and Depression Scale.
*
p < 0.05.
**
p < 0.01.

stroke period and may share common underlying mechanisms.

Table 4
Multivariate stepwise regression analysis for each dimension of MFI. Staub and Bogousslavsky (2001) suggested PSF can be divided into
various subtypes (i.e., physical, somatic fatigue, mental, or
b P VIF Adjusted
psychological), and postulated the concept of ‘primary’ post stroke
R2
fatigue, which may develop in the absence of depression or a
General fatigue 0.51 <0.001 1.006 0.397
significant cognitive sequel and which may be linked to attentional
Anxiety 0.34 <0.001 1.018
Lesion side 0.23 0.016 1.015 deficits due to the interruption of neural attentional networks.
Lesion location Multivariate stepwise regression analysis found that among the
Physical fatigue 0.33 0.001 1.042 0.330 clinical variables, right side lesions were associated with general
Lesion side 0.33 0.002 1.128 and physical fatigue, and thalamus and brainstem lesions were
Depression 0.24 0.018 1.070
Diabetes mellitus Anxiety 0.24 0.019 1.079
associated with general fatigue. The relationship between lesion
Reduced activity 0.40 0.001 1.000 0.145 location and PSF is unclear (Choi-Kwon and Kim, 2011). Most
Depression studies found no association. In contrast, several studies found
Reduced motivation 0.56 <0.001 1.031 0.303 associations with specific brain structures, such as the thalamus,
Depression 0.25 0.016 1.031
brainstem (Staub and Bogousslavsky, 2001), or basal ganglia (Tang
BMI
Mental fatigue 0.52 <0.001 1.039 0.278 et al., 2010). A brainstem fatigue generator model has been
Depression 0.30 0.004 1.039 postulated (Staub and Bogousslavsky, 2001; Chaudhuri and Behan,
Diabetes mellitus 2004). Structural lesions that disrupt cortical activating systems
VIF, Variance Inflation Factor; MFI, Multidimensional Fatigue Inventory; BMI, Body are implicated in the pathophysiological process of PSF. In addition
mass index. to lesions, right hemispheric stroke would be associated with PSF
(Manes et al., 1999). Many neuropsychiatric syndromes, including
anxiety, are also associated with right brain lesions (Aström, 1996).
depression was compatible with previous studies (Whyte and As Wu et al. (2015) mention in their review, in studies where PSF
Mulsant, 2002). Higher levels of depression were also associated and lesion site showed significant association, fatigue was usually
with higher levels of fatigue, especially reduced motivation, assessed within the first few months after stroke.
reduced activity, and mental fatigue, though less in general and In contrast to previous studies, no statistically significant
physical fatigue. Anxiety was significantly correlated with general association between PSF and functional and cognitive impairment
and physical fatigue. Many studies reported robust relationships was observed in multivariate stepwise regression analyses. Total
between PSF and depression (Choi-Kwon et al., 2005; Lerdal et al., FIM score was only correlated with MFI reduced activity.
2011; Kutlubaev et al., 2013), Since subjective fatigue is a Functional deficits are reported to be one of the most important
multidimensional state, the strong relationships between depres- causes of PSF (Glader et al., 2002; Christensen et al., 2008).
sion and reduced motivation, reduced activity, and mental fatigue However, many previous studies investigated patients in the
seen in this study may represent psychological components of PSF. chronic period, and functional state may have greater impact on
The relationship between PSF and anxiety has been less later fatigue.
frequently investigated. A systematic review suggested a trend We also found significant but relatively weak associations
toward association between PSF and anxiety, but this association between diabetes mellitus and both physical and mental fatigue,
was weak after controlling for the effect of depressive symptoms and between BMI and reduced activity. Considering the patho-
(Wu et al., 2014). On the contrary, we found anxiety was the best physiology of PSF, the influence of comorbidities is not negligible,
predictor for general and physical fatigue in the acute period. The since comorbid medical conditions or malnutrition are potential
relationships between anxiety and PSF seem to be somewhat causes of fatigue. Impact of diverse comorbidities on PSF has rarely
different from depression and PSF, since anxiety were less likely to been investigated (Choi-Kwon and Kim, 2011).
manifest as general or physical components of PSF. To our A major strength of this study is that anxiety and depression are
knowledge, this is the first report indicating that anxiety and differently correlated with physical and mental aspects of PSF in
depression are independently correlated with multidimensional early stroke patients. These results indicate the need for clinicians
aspects of PSF in the acute phase. Interestingly, the relationships to consider the complexity between affective symptoms and PSF
between anxiety and PSF are mostly noted within early periods and needs for effective intervention of affective symptoms in
after stroke (Snaphaan et al., 2011; Radman et al., 2012; Kutlubaev fatigued stroke survivors.
et al., 2013; Duncan et al., 2015). Furthermore, Duncan et al. (2015)
reported that anxiety at 1 month was an independent predictor for 4.1. Limitations
increased PSF at 6 and 12 months. Several explanations are possible
for this. Anxiety and depression may be co-occurring sequelae of Several study limitations should be acknowledged. Our sample
stroke, and anxiety in the acute phase may predispose patients to size was relatively small to generalize the results. A potential
later depression (Sagen et al., 2010). Both anxiety and fatigue may source of bias is the consecutive series of stroke patients with high
also be direct consequences of brain damage in the early post average age, many of whom had a recurrence, and we excluded
 H. Mutai et al. / Asian Journal of PsychiatryAJP 26 (2017) 1–5
severe aphasic stroke and so more right side lesion patients were
included, which might influence results. This study did not include
possible predisposing variables, such as prestroke fatigue or
premorbid mood. Considering the complexity of PSF, collection of
more detailed data and the performance of further studies would
be needed to elucidate factors related to PSF.
4.2. Conclusions
PSF was highly prevalent and associated with anxiety within 2
weeks after stroke. Right side lesions and thalamic and brainstem
lesions were associated with PSF. Further study is needed to
elucidate how specific structural lesions and anxiety relate to the
development of early PSF.
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