Inactive lifestyles and sedentary behavior in persons with chronic aneurysmal subarachnoid hemorrhage: evidence from accelerometer-based activity monitoring
Harmsen et al. Journal of NeuroEngineering and Rehabilitation
Inactive lifestyles and sedentary behavior in persons with chronic aneurysmal subarachnoid hemorrhage: evidence from accelerometer-based activity monitoring
Wouter J. Harmsen 0 1
Gerard M. Ribbers 0 1
Majanka H. Heijenbrok-Kal 0 1
Johannes B. J. Bussmann 0 1
Emiel M. Sneekes 0 1
Ladbon Khajeh 2
Fop van Kooten 2
Sebastian J. C. M. M. Neggers 3
Rita J. van den Berg-Emons 0 1
0 Department of Rehabilitation Medicine, Erasmus MC University Medical Center Rotterdam , P.O. Box 2040, 3000, CA, Rotterdam , The Netherlands
1 Rijndam Rehabilitation Institute , Rotterdam , the Netherlands
2 Department of Neurology, Erasmus MC University Medical Center Rotterdam , Rotterdam , the Netherlands
3 Department of Endocrinology, Erasmus MC University Medical Center Rotterdam , Rotterdam , the Netherlands
Background: Aneurysmal subarachnoid hemorrhage (a-SAH) is a potential life-threatening stroke. Because survivors may be at increased risk for inactive and sedentary lifestyles, this study evaluates physical activity (PA) and sedentary behavior (SB) in the chronic phase after a-SAH. Methods: PA and SB were objectively measured at six months post a-SAH with an accelerometer-based activity monitor, with the aim to cover three consecutive weekdays. Total time spent in PA (comprising walking, cycling, running and non-cyclic movement) and SB (comprising sitting and lying) was determined. Also, in-depth analyses were performed to determine the accumulation and distribution of PA and SB throughout the day. Binary time series were created to determine the mean bout length and the fragmentation index. Measures of PA and SB in persons with a-SAH were compared to those in sex- and age-matched healthy controls. Results: The 51 participants comprised 33 persons with a-SAH and 18 controls. None of the participants had signs of paresis or spasticity. Persons with a-SAH spent 105 min/24 h being physically active, which was 35 min/24 h less than healthy controls (p = 0.005). For PA, compared with healthy controls, the mean bout length was shorter in those with a-SAH (12.0 vs. 13.5 s, p = 0.006) and the fragmentation index was higher (0.053 vs. 0.041, p < 0.001). Total sedentary time during waking hours showed no significant difference between groups (514 min vs. 474 min, p = 0.291). For SB, the mean bout length was longer in persons with a-SAH (122.3 vs. 80.5 s, p = 0.024), whereas there was no difference in fragmentation index between groups (0.0032 vs 0.0036, p = 0.396). Conclusions: Persons with a-SAH are less physically active, they break PA time into shorter periods, and SB periods last longer compared to healthy controls. Since inactive lifestyles and prolonged uninterrupted periods of SB are independent risk factors for poor cardiovascular health, interventions seem necessary and should target both PA and SB. Study registration: Dutch registry number: NTR 2085.
Subarachnoid hemorrhage; Physical activity; Sedentary behavior; Fatigue; Rehabilitation; Stroke
Aneurysmal subarachnoid hemorrhage (a-SAH) is
defined by the extravasation of blood into the
subarachnoid space, and is caused by a spontaneous bleeding of a
ruptured brain aneurysm [
]. It accounts for 5% of all
stroke cases and has an incidence rate of 9/100,000
persons/year and a mortality rate of 50% [
Persons with a-SAH are relatively young compared
with those with ischemic or hemorrhagic stroke
(55 years vs. 70 years) [
]. Further, whereas
ischemic or hemorrhagic stroke may lead to focal brain
injury with specific stroke-related symptoms, brain
injury in a-SAH has a more diffuse character without
typical stroke symptoms [
]. Those who survive are
likely to experience long-term symptoms, such as
cognitive problems (40%), emotional complaints
(50%), depressive symptoms (40%), and fatigue (up to
]. Even among those who are classified as
having a ‘favorable outcome’, the incidence of clinical
deficits is high .
Persons with a-SAH seem to have difficulty with
resuming their daily activities, and only one-third is able
to fully resume their previous occupation [
inability to perform daily activities is associated with
passive coping styles, depressive symptoms and fatigue
]. Reduced physical fitness after a-SAH has been
]. which may also hinder the performance
of daily activities. Therefore, individuals with a-SAH
may be at risk of inactive and sedentary lifestyles,
placing them at risk for poor health outcomes [
However, measures of daily PA and SB have not yet been
studied after a-SAH.
PA refers to ‘any bodily movement produced by skeletal
muscles that requires energy expenditure’ and contributes
to the primary and secondary prevention of chronic
diseases, including cardiovascular disease, cancer, diabetes
mellitus, hypertension and obesity [
]. SB, defined
as a distinct class of activities that requires low levels of
energy expenditure and involves sitting and lying
activities during waking hours, negatively impacts
metabolism and cardiovascular health [
]. Recent studies
show that SB impacts cardiovascular health, independent
of the volume of PA [
]. Furthermore, not only the
total volume of PA or SB, but also the way PA and SB
are accumulated is important, i.e. prolonged bouts of PA
are beneficial, whereas prolonged bouts of SB are found
to be detrimental to cardiovascular health [
Persons with stroke not caused by a-SAH are highly
sedentary, with PA levels almost half that of healthy
control subjects [
]. In stroke rehabilitation, improving
PA and SB is strongly recommended, as it provides
protective benefits in the primary and secondary prevention
of chronic diseases [
]. Inactive and sedentary
lifestyles in ischemic or hemorrhagic stroke have been
frequently explained by motor impairments following
neuro-motor lesions. Since brain injury in a-SAH is
more diffuse without typical stroke symptoms (such as
paresis), it would be of interest to gain insight in the
level of PA and SB in this patient group.
Despite its importance, PA and SB have not yet been
studied in persons with a-SAH. Therefore, this study
evaluates PA and SB in the chronic phase after a-SAH.
Objectively obtained measures of PA and SB were
compared to those in sex- and age-matched healthy
controls. This study can help to optimize recommendations
to prevent chronic diseases and debilitating conditions
after a-SAH, but can also be used to better understand
the consequences of different types of stroke on daily PA
and SB. Since individuals with a-SAH have difficulty in
resuming their daily activities and have reduced physical
fitness, we hypothesized that they would be less
physically active and more sedentary compared to healthy
Participants and study design
The present study (entitled HIPS-Rehab) was part of the
‘Hypopituitarism In Patients after Subarachnoid
hemorrhage (HIPS) study’ [
]. In this study we
investigate the PA and SB of persons who were six months
post a-SAH. Participants with a-SAH admitted to the
department of Neurology of Erasmus University MC were
eligible for inclusion if they were aged ≥18 years.
Diagnosis of a-SAH was confirmed by computerized
tomography (CT) of the brain and, in cases with negative CT,
by lumbar puncture. Exclusion criteria were:
hypothalamic or pituitary disease diagnosed prior to a-SAH,
history of cranial irradiation, trauma capitis prior to a-SAH,
other intracranial lesion apart from a-SAH, and other
medical or psychiatric condition or laboratory
abnormality that may interfere with the outcome of the study.
Participants were also excluded if they were aged
≥70 years. For comparison, we included healthy controls
of similar sex (% females; 64 vs. 72%, p = 0.382) and age
(52.6 vs. 51.0 years, p = 0.548). Healthy controls were
recruited by advertisement; they wore identical activity
monitors and similar measurement procedures were
The study was approved by the Medical Ethics
Committee of Erasmus University Medical Centre, and
all participants provided written informed consent.
Physical activity and sedentary behavior
PA and SB were objectively measured with an
accelerometer-based activity monitor (VitaMove)1 (Fig. 1).
This monitor has demonstrated validity for quantifying
body postures and movements in healthy subjects and in
different patient groups [
]. The VitaMove activity
monitor consists of three individual body-fixed recorder
units, which are wirelessly connected and synchronized
every 10 s. One recorder unit was attached to the trunk
(sternum position) and one to each thigh, using specially
developed elastic belts. Each unit has its own tri-axial
accelerometer,2 power supply and storage capacity.
Participants wore the VitaMove on consecutive weekdays, except
during swimming, bathing and sleeping. In line with
previous research, the intended duration of measurement
was three consecutive days, with a minimum of one day
]. Further, the signal processing parameters were
identical to the parameter settings used in previous
validity studies [
]. Mean values were calculated for
multiple days of activity monitoring. Participants were
instructed to continue their ordinary daily activities. The
principles of the measurements were explained after all
measurements were completed in order to avoid
measurement bias. In addition, participants kept activity diaries to
report reasons of non-wear periods of the activity monitor.
Accelerometer signals of each recorder unit were
continuously measured and stored (128 Hz) on a micro
Secure Digital memory card. Accelerometer signals were
downloaded on a computer for kinematic analyses using
specially developed VitaScore software.3 Waking hours
were determined by the researcher (WH) using the
diaries filled out by the participants and by inspection of the
raw data signals; specifically, ongoing flatlines indicate
that the recorder units were taken off, reflecting the end
of waking hours. Body postures and movements (e.g.
lying, sitting, standing, walking, cycling, running and
non-cyclic movements) were automatically detected with
a 1-s time resolution from the feature time series (i.e.
angle, frequency and motility) derived from the
measured accelerometer signals. The motility feature
expresses the intensity of the movement of the body
segment to which the unit is attached, and depends on
the variability of the acceleration signal; motility can be
compared to counts that are calculated in regular
activity monitors (calculated in gravitational force (g),
1 g = 9.81 m/s2). During walking, the body motility
signal (i.e. the mean of the leg and trunk motility signals)
corresponds to walking speed [
]. The minimum
duration threshold for each activity was 5 s. A detailed
description of the algorithms and analysis is published
In-depth analyses were performed to quantify the
accumulation and distribution metrics of PA and SB. For
PA outcomes, the four detected body movements
(walking, cycling, running, and non-cyclic movements)
were categorized into one PA category; a similar
procedure was followed for the SB category, covering lying and
sitting activities. Binary time series of PA (yes = 1, no = 0)
and SB (yes = 1, no = 0) were created using
custommade Matlab algorithms. A period of uninterrupted
samples of either PA (or SB) was classified as a bout.
Due to the minimum duration threshold of 5 s, bouts
and periods between bouts lasted at least 5 s.
Volume, intensity and distribution of PA and SB
To determine the volume of PA, we calculated the total
time spent in the four detected body movements during
waking hours. The volume of total SB was determined
by evaluating the total time of sitting and lying activities
during the waking hours. Volume measures were then
expressed as a percentage of a 24h period, and as a
percentage of waking hours. The mean motility of PA
and the mean motility of walking were also determined
and expressed in g.
The binary time series were used to determine the
accumulation and distribution of PA and SB. The total
number of bouts and the mean bout length (in seconds)
were calculated. Since the mean bout length was not
normally distributed, the natural logarithm was taken.
The mean log length was back transformed to the
original scale. The fragmentation index was calculated
and reflects the ratio between the number of PA (or SB)
bouts divided by the total PA (or SB) time [
]. A higher
fragmentation index indicates that total PA (or SB) time
is more fragmented, which means that there are less
prolonged periods of PA (or SB) [
At hospital intake, the following Clinical characteristics
were obtained including: 1) the severity of a-SAH
according to the grading of the World Federation of
Neurologic Surgeons (low-grade: I-III or high-grade:
] and the Glasgow Coma Scale (GCS) score,
 2) location of the aneurysm (anterior or posterior
circulation), 3) treatment procedure (surgical clipping
or endovascular treatment), 4) presence of secondary
health complications (re-bleed, delayed cerebral
ischemia, hyponatremia, hydrocephalus and growth
hormone deficiency; defined as an insufficient growth
hormone (GH) response to a GH-releasing hormone
-arginine test), [
] and 5) neurologic comorbidity
(paresis or spasticity). Neurologic morbidity (such as
paresis or spasticity) was evaluated by treating neurologist.
Information on the following characteristics and body
anthropometrics were collected from both groups: sex,
age, weight, height and Body Mass Index (BMI).
All data are expressed as mean (SD) unless otherwise
indicated. To compare the clinical characteristics between
participants of HIPS-Rehab and those who did not
participate (but were included in HIPS), we used
independent t-tests for continuous data and chi-square-tests
for categorical data. To compare the characteristics and
measures of PA and SB between individuals with a-SAH
and controls, independent t-tests were applied for
continuous data and chi-square tests for categorical data.
All analyses were performed using IBM SPSS Statistics,
version 20.4 A probability value of p < 0.05 was
considered statistically significant.
Of the 241 patients admitted to the ICU with a diagnosis
of a-SAH, 84 were included in HIPS of which 52
volunteered to participate in HIPS-Rehab. Participants in
HIPS-Rehab (n = 52) did not differ from those who did
not participate (but were included in HIPS; n = 32)
regarding the severity of a-SAH, location of the aneurysm,
treatment procedure, and the presence of secondary
health complications. Of the 52 participants, successful
activity monitoring measurements were obtained from
33: of the 19 unsuccessful attempts, 6 refused to wear
the activity monitor, in 4 persons data processing was
unsuccessful due to technological failure, and 9 were
aged ≥70 years (Fig. 2).
Table 1 presents the clinical characteristics. Most
persons underwent endovascular coiling (82%) and had a
ruptured aneurysm in the anterior circulation (61%).
The neurological scores showed that 29 participants had
a low-grade a-SAH (88%) and a mean GCS score of 14.0
(SD 2.0). None of the participants had a paresis or
showed signs of spasticity.
Due to challenges with activity monitoring, data were
not available for all participants for the intended three
days of measurement. The duration of measurement was
3 days in 42% of those with a-SAH and in 83% of the
controls; 2 days in 48% of those with a-SAH and in 6%
of the controls; and 1 day in 9% of the persons with
aSAH and in 11% of the controls. Mean daily wear
time did not differ between the groups, 13.7 h (SD
1.8) vs. 14.1 h (SD 1.3), respectively, (95% CI of the
difference: −1.4 h to 0.5 h; p = 0.372).
Table 2 presents the characteristics of the two groups:
persons with a-SAH did not differ from healthy controls
regarding sex (p = 0.382), age (p = 0.548), weight
(p = 0.231) and height (p = 0.062), but had a higher BMI
(p = 0.002). Table 2 also presents the volume measures
of PA and SB in the two groups. Persons with a-SAH
spent 105 min/24 h (=7.3%) being physically active,
which is 35 min/24 h (2.4%) less compared with that of
healthy controls (140 min/24 h (=9.7%); p = 0.005); in
particular, there was less participation in cycling
activities (3 min/24 h (=0.2%) vs. 27 min/24 h (=1.9%);
p < 0.001). Total sedentary time did not differ between
those with a-SAH and healthy controls; 514 min/24 h
(=35.7%) vs. 473 min/24 h (=32.9%; p = 0.291),
respectively. Also, there was no difference between the groups
in total standing time, i.e. 200 min/24 h (=13.9%) vs.
233 min/24 h (=16.2%, p = 0.164), or in mean PA
motility and mean walking motility (p = 0.442 and p = 0.503,
Mean bout length of PA in persons with a-SAH was
shorter than in controls (12.0 s vs. 13.5 s; p = 0.006),
and the PA fragmentation index was higher (0.053 vs.
0.041; p < 0.001), indicating that the PA periods were
shorter and the total time spent in PA was more
fragmented in persons with a-SAH. Mean bout length of SB
was longer in persons with a-SAH (122.3 s vs. 80.5 s;
p = 0.024), whereas the SB fragmentation index did not
differ between groups (p = 0.396). This indicates that SB
periods lasted longer in persons with a-SAH, but the
way in which the total SB was distributed did not differ
between groups (Table 3).
The present study shows that persons with a-SAH are
less physically active, they break PA time into shorter
periods, and SB periods last longer compared to healthy
controls, placing them at increased risk for poor health
]. This is the first study on PA and SB in
persons with a-SAH. The objectively obtained measures of
PA and SB have meaningful implications for stroke
rehabilitation because our findings reveal that inactive and
sedentary lifestyles are present in absence of motor
impairments. Given the importance of optimal PA and SB,
] therapeutic interventions are warranted. The
present findings may help to improve interventions
(targeting both PA and SB) and prevent debilitating
conditions after a-SAH.
In-depth analysis of PA revealed that persons with
aSAH break their PA time into shorter periods, which is
not beneficial from a health perspective [
interruptions may be explained by an increased number of
moments of rest, possibly related to higher fatigability,
cognitive dysfunction, and/or lower cardiorespiratory
]. The most recent guidelines of the WHO
recommend an accumulation of PA time, i.e. uninterrupted
PA, of at least 10 min, as this is an important aspect of
healthy PA . Therefore, therapeutic interventions
should not only target the total volume of PA, but
should also improvethe accumulation of PA time in
persons with a-SAH.
Sedentary time, particularly accumulated in long
uninterrupted periods, negatively impact cardiovascular
health, independent of the volume of PA [
analysis of SB revealed that SB periods lasted longer in
persons with a-SAH. However, the SB fragmentation
index did not differ, indicating that the way total SB is
distributed in a-SAH is similar to that in healthy
controls. This could be explained by the fact that the total
sedentary time was somewhat higher (albeit not
significant) in a-SAH than in healthy controls. Since SB
periods lasted longer in those with a-SAH than in controls,
breaking prolonged uninterrupted SB periods may
represent another therapeutic target in order to provide
additional health benefits in persons with a-SAH.
In patients with stroke not caused by a-SAH, the most
commonly used objective measures of PA are step or
activity counts per day; these counts are reported to be
almost half those of healthy controls [
]. The present
study explored activity profiles beyond simple step or
activity counts and distinguished different types of PA.
Overall, persons with a-SAH spent 25% less time in PA than
healthy controls (105 vs 140 min/24 h, respectively).
However, the total volume of walking activities did not differ
between groups; this is in line with an
accelerometerbased study on walking activities in patients with stroke
]. Furthermore, compared with controls, persons with
a-SAH participated particularly less in cycling activities
and, to a lesser extent, in running activities.
Interestingly, physically inactive and sedentary
lifestyles after a-SAH seem not be related to motor
impairments, and therefore other mechanisms should underlie
our findings. For example, PA may be limited by
impaired cardiorespiratory fitness, cognitive dysfunction,
anxiety or fatigue. Feelings of anxiety after a-SAH can
highly restrict participation in daily activities [
Furthermore, PA can also be limited by concentration
5, 43, 44
] e.g. cycling activities are more
demanding due to participation in traffic and multitasking.
However, future studies are warranted to investigate the
barriers and facilitators of PA after a-SAH, and should
take into account mechanisms of physical
deconditioning, cognitive dysfunction, anxiety and fatigue.
In persons with a-SAH, total sedentary time during
waking hours was 514 min. This is similar to findings in
persons with stroke, not caused by a-SAH (i.e. sedentary
times ranging from 464 to 654 min) [
]. This is
remarkable because patients with a non a-SAH stroke
are often older and more restricted in the performance
of daily activities (often because of neurological deficits)
than patients with a-SAH [
]. With regard to SB, there
are no guidelines for the general population. A
metaanalysis showed that above 7.0 h, every additional hour
increase in SB time is associated with a 5% increase in
all-cause mortality [
]. In the present study, individuals
with a-SAH spent about 8.5 h being sedentary, implying
a 7.5% increase in all-cause mortality. In order to set
therapeutic targets, additional studies are needed to
establish guidelines for SB.
The major strength of the present study is the
objective measurement of PA and SB, without possible
bias from the subjective character of a questionnaire.
Also, the inclusion of healthy controls allowed us to
better interpret the data. Another strength is that we
used innovative in-depth analyses of PA and SB which
provides new insights to support future therapeutic
Some limitations of the present study should be
discussed. First, we used an advanced activity monitor that
allowed to obtain continuous data on various types of
PA and SB. However, this makes it difficult to compare
our data with general guidelines for healthy PA or SB,
because these guidelines are mostly based on self-report
]. Future studies need to define
guidelines for healthy PA and SB, based on objectively
obtained measures. Second, for logistic reasons, the sample
size of healthy controls was smaller compared to that in
persons with a-SAH. Smaller number of controls have
been frequently reported in activity monitoring research
across different patient groups, including stroke [
Overall, results on the main outcome (volume metrics)
Duration of activities as a percentage of 24 h
aPhysical behavior was monitored on consecutive weekdays in the free-living situation
bNon-wear = time that participants did not wear the activity monitor (also reflects nighttime)
cg = gravitational forces *100
in the controls are comparable with, and for PA even
somewhat lower (9.7% vs 10–12% per 24 h, respectively)
than results, as measured with the VitaMove, in other
healthy comparison groups [
]. This difference may
even indicate that we have underestimated the lack of
PA in persons with a-SAH. BMI was somewhat higher in
persons with a-SAH than in controls. However, it was
not feasible to account for BMI, as a higher BMI may
already be indicative of physically inactive and sedentary
lifestyles. Another limitation is that, in both groups,
actually ‘wearing’ the activity monitor may have influenced
PA in daily life; nevertheless, all participants reported
that they performed their regular PA. Another limitation
is that we did not include any physiological parameters
(e.g. heart rate) that might have provided more details
on physical strain of PA in daily life.
Objectively obtained measures of PA and SB show
that persons with a-SAH are less physically active,
they break PA time into shorter periods, and SB
periods last longer compared to healthy controls.
These results suggest that persons with a-SAH have
increased health risks related to inactive lifestyles and
sedentary lifestyles. Given the importance of optimal
PA and SB, future studies need to identify barriers
Controls (n = 18)
95% CI of the difference
−2.4 to −0.4
0.006 to 0.019
5.6 to 78.0
The minimum bout length lasted at least 5 s
aUninterrupted bouts with a minimum length of 5 s
bFragmentation index represents the ratio between the number of sedentary bouts divided by the total time being sedentary
and facilitators of PA and SB to develop optimal
therapeutic interventions to improve PA and SB after
1Activity Monitor, VitaMove, 2 M Engineering,
Veldhoven, the Netherlands
2Accelerometer, Freescale MMA7260Q, Denver, USA
3Activity monitor software, VitaScore BV, Gemert, the
4SPSS Inc., Chicago, IL, USA
Financial support for this study was provided by the Dutch Brain Foundation
(grant no. 15F07.06).
Availability of data and materials
The dataset used and/or analyzed during the current study available from
the corresponding author on reasonable request.
WH contributed to the data collection, data analysis and drafting of the
manuscript; GR and RB contributed to the design, data analysis, data
interpretation and drafting of the manuscript; MH contributed to the design,
statistical analysis and manuscript review; JB contributed to the
interpretation of the data and manuscript review; ES contributed to the data
collection, data analysis and manuscript review; LK, FK and SN contributed to
the design, data interpretation and manuscript review. All authors read and
approved the final manuscript.
Ethics approval and consent to participate
The present study was approved by the Medical Ethics Committee of
Erasmus Medical Centre (Dutch Registry: NTR 2085). All participants provided
written informed consent in accordance with ethical guidelines.
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
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