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Disabil Rehabil, Early Online: 1–9

! 2014 Informa UK Ltd. DOI: 10.3109/09638288.2014.966162

RESEARCH PAPER

Early rehabilitation in patients with acute aneurysmal subarachnoid

hemorrhage
Tanja Karic1,2, Angelika Sorteberg2, Tonje Haug Nordenmark1, Frank Becker3,4, and Cecilie Roe1,4
1
Department of Physical Medicine and Rehabilitation, Oslo University Hospital, Ullevaal, Nydalen, Oslo, Norway, 2Department of Neurosurgery,
Oslo University Hospital, Rikshospitalet, Nydalen, Oslo, Norway, 3Sunnaas Rehabilitation Hospital, Bjørnemyrveien, Nesoddtangen, Norway,
Disabil Rehabil Downloaded from informahealthcare.com by McMaster University on 02/27/15

and 4Institute of Clinical Medicine, University of Oslo, Oslo, Norway

Abstract Keywords
Purpose: The aim of this study was to describe and quantify the content of early rehabilitation Brain injury, early rehabilitation, intracranial
adapted to patients with acute aneurysmal subarachnoid hemorrhage (aSAH) and to assess its aneurysm, mobilization, stroke,
feasibility. Methods: This was a prospective, observational study including 37 aSAH patients. subarachnoid hemorrhage
Early rehabilitation was applied according to a mobilization algorithm. Clinical parameters, the
time that rehabilitation team used on early rehabilitation and progression in mobilization were History
recorded. The patients’ clinical conditions were graded according to the World Federation of
Neurological Surgeons scale (WFNS). Results: Poor-grade patients (WFNS 3, 4, 5) (n ¼ 12) Received 25 January 2014
received more rehabilitation (median 412 min) than did good-grade patients (WFNS 1, 2) Revised 1 August 2014
For personal use only.

(median 240 min). Mobilization to 60 of head elevation in good-grade patients began on day Accepted 12 September 2014
one after securing the aneurysm. Out-of-bed mobilization was possible on day three. Poor- Published online 29 September 2014
grade patients were mobilized to 60 after two days and were out of bed on day seven. At
discharge, 67% of poor-grade patients were mobilized to walking versus 78% of good-grade
patients. No serious adverse effects to early rehabilitation were observed. Conclusions: Early
rehabilitation in aSAH patients is feasible from the first day after securing the aneurysm. The
rehabilitation content varied according to the patient’s clinical grade.

ä Implications for Rehabilitation

 Early rehabilitation is feasible from the first day after securing the ruptured aneurysm in
patients with aneurysmal subarachnoid hemorrhage (aSAH).
 Early rehabilitation requires close monitoring and continuous adjustment for the content and
amount according to the patient’s clinical condition.
 Interdisciplinary collaboration is recommended to match the rehabilitation needs to the
medical condition on a daily basis.

Introduction management of patients with aSAH focuses on the reduction of

secondary brain damage and the prevention of further neuro-
Aneurysmal subarachnoid hemorrhage (aSAH) is a life-threaten-
logical injury. Aneurysmal rebleeding, hydrocephalus, cerebral
ing condition accounting for approximately 3–5% of all strokes,
vasospasm and seizures represent the most severe secondary
with half of the patients being younger than 55 years [1,2]. The
complications [1]. Pneumonia, meningitis, electrolyte abnormal-
incidence rate ranges from 4 to 10 per 100 000 person-years in
ities and thrombosis represent common medical complications
most countries. In Norway, the incidence rate of aSAH is
[1]. Together with critical illness myeloneuropathy, these com-
approximately 10.0 per 100 000 person-years [3].
plications contribute to the burden of care in the acute phase.
Early securing of the aneurysm, more aggressive drainage of
Long-term problems in survivors of aSAH include physical,
cerebrospinal fluid (CSF) and improved neurointensive care have
emotional and cognitive difficulties, contributing to limitations in
resulted in better survival rates [4,5], but the case fatality remains
activities and participation in social activities and work [8,9].
high. In the last three decades, the case fatality rate for aSAH in
In non-SAH stroke care and traumatic brain injury (TBI) care,
Norway at 1, 3, 7 and 30 days was 14%, 20%, 24% and 36%,
early rehabilitation has been established as an integral part of
respectively [6]. Cerebral ischemia is considered a crucial risk
acute and sub-acute treatment, resulting in reduced mortality,
factor for poorer neurological outcome and increased case fatality
fewer complications and better functional outcomes [10–17].
[7]. After the early securing of the aneurysm, intensive care
Current recommendations in rehabilitation after acute ischemic
stroke include mobilization out of bed as early as possible [18].
Address for correspondence: Dr Tanja Karic, Department of Physical However, there remains a need for a consensus on what type
Medicine and Rehabilitation, Oslo University Hospital, Ullevaal, P.B. of rehabilitation with what content and dose should be imple-
4950 Nydalen, Oslo 0424, Norway. E-mail: tanja.karic@gmail.com mented early in different patients groups [19,20]. Thus, early
 2 T. Karic et al.
rehabilitation after aSAH represents one of the most challenging
areas in rehabilitation medicine due to the assumption that
increased activity can adversely affect intracranial pressure (ICP)
and/or arterial blood pressure (ABP) and hence reduce the
cerebral perfusion pressure (CPP). These processes may poten-
tially trigger deleterious secondary brain damage. In particular,
the exacerbation of cerebral vasospasm and consecutive delayed
ischemic neurologic deficit (DIND) is a concern, prompting the
prescription of bed rest in the early period after aSAH. However,
bed rest has not been proven to prevent cerebral vasospasm and/or
ischemia [21].
As the effect of early rehabilitation on functional outcomes
after stroke and TBI is well documented and beneficial, early
rehabilitation should not be withheld in patients with aSAH.
Hence, this study aimed to describe the content and feasibility of
early rehabilitation adapted to aSAH patients. We present a novel
protocol for mobilization in aSAH patients. The effectiveness of
early rehabilitation in aSAH patients with regard to the frequency
of complications and functional outcome is beyond the scope of
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this paper.
Materials and methods
This prospective, observational study is part of a larger project
titled ‘‘The effect of early rehabilitation after aneurysmal SAH’’
and was approved by the Regional Committee for Medical
Research Ethics, Southeast Norway in January 2012, archive
number 2011/2189, Clinical Trials number 0925-0586 (Clinical
Trials Gov. identifier NCT01656317). Oral and written consent
was obtained from all the patients included in the study.
For personal use only.
Research context
Oslo University Hospital (OUS) is the primary hospital for the
southeast health region in Norway for the treatment of patients
with non-traumatic SAH, serving 2.7 million inhabitants. Patients
are referred to the Department of Neurosurgery after the diagnosis
of SAH at their local hospital and are discharged back to the local
hospital as soon as the acute neurosurgical treatment is
completed. There is a 24/7 service of surgical and endovascular
aneurysm repair performed by a dedicated vascular team. All
aSAH patients are treated with early securing of the aneurysm.
Patients are treated at the general intensive care unit (ICU) under
neurosurgical supervision as long as they require invasive
mechanical respiratory support. Thereafter, patients are trans-
ferred to the neuro-intermediate ward (NIW), which is an
intensive care unit taking care of patients in need of noninvasive
respiratory support. Patients who need prolonged care in the ICU
but no further neurosurgical care were directly transferred to the
ICU at their respective local hospital.
Patients
We included patients with aSAH who were treated at the NIW
between August and December 2012 after securing of their
ruptured aneurysm. Exclusion criteria: age 518 years, unsecured
ruptured aneurysm, patients with previous SAH, brain injury or
neurodegenerative disorder, and end of life care (no early
rehabilitation applied). Information on medical history was
gathered from a detailed search through all the medical records.
Clinical and radiological variables
The World Federation of Neurological Surgeons (WFNS) scale
[22] was used for grading the clinical condition of patients on
arrival at the NIW.
We registered the mode of securing the aneurysm, the use of
CSF drainage through an external ventricular drain (EVD),
Disabil Rehabil, Early Online: 1–9
lumbar drain (LD), and ventriculo-peritoneal shunt (VP-shunt) as
well as the use of an intracranial pressure (ICP) sensor. We also
registered the length of stay at the ICU and NIW.
Early rehabilitation
Early rehabilitation had been integrated into acute care with a
common understanding and holistic view of all aspects of the
patient’s care. The early rehabilitation team had an inter-
disciplinary approach [23] and consisted of a rehabilitation
physician, a neurosurgeon, a physical therapist (PT), an occupa-
tional therapist (OT) and nurses with special expertise within the
care of vascular neurosurgical patients. A clinical neuropsych-
ologist, speech therapist and medical social workers were also
available. The entire early rehabilitation team defined rehabilita-
tion goals and the maximum mobilization level every morning
after the examination of the patient and the assessment of
surveillance parameters.
All the patients received the usual acute care according to
aSAH guidelines throughout the day. Early rehabilitation by the
rehabilitation team was performed during daytime (working
hours: 8:00 a.m.–03:00 p.m.), five days per week. The recom-
mendations and defined goals set by the rehabilitation team were
continued by the nurses during evenings and week-ends as part of
their routine. The OT was available two days each week during
the daytime. Both the PT and OT were experienced in the early
rehabilitation of patients after severe TBI [12] and adjusted early
rehabilitation principles from TBI rehabilitation to the aSAH
patients. The early rehabilitation program was specially designed
for aSAH patients. Early rehabilitation in patients after TBI in
Denmark [24] and Sweden [13] served as sources of inspir-
ation for our early rehabilitation program but needed modifica-
tion in order to be applicable on patients in the acute state
of aSAH.
For analyses purpose, the content of early rehabilitation was
divided into 10 categories:
(1) Positioning in neutral during rest and sleep (Positioning)
(2) Passive exercises for contracture prevention (Passive
exercises)
(3) Pulmonary rehabilitation
(4) Guidance in activities of daily living (ADL), with the
exception of swallowing and eating
(5) Assessment and guidance in swallowing and eating
(Swallowing and eating)
(6) Mobilization and transfers from bed to chair and to the
standing position (Mobilization)
(7) Stimulation to activity and body exercises (Activation)
(8) Balance training (Balance)
(9) Reality orientation
(10) Information and emotional support to patients and their
families (Information)
In patients with a neurological deficit and/or significantly
decreased consciousness, early rehabilitation comprised passive
exercises for contracture prevention and appropriate positioning
during rest and sleep. The main purpose was to prevent pressure
ulcers, decrease spasticity, prevent the development of joint
deformities, facilitate respiration and prevent pulmonary compli-
cations. Rehabilitation was also based on sensory stimulation and
guided movements to facilitate activities of daily living (ADL),
often applied in the morning in conjunction with personal hygiene
and dressing. Patients were inspired to contribute, and the tasks
were solved in collaboration with the patients.
The PT and OT performed assessments and guidance in
swallowing and eating and provided recommendations on the
appropriate body positioning during meals and on the consistency
and quantity of food.
 DOI: 10.3109/09638288.2014.966162
All patients received a Lung flute and respiratory as well as
general body exercises adapted to their clinical condition.
Balance training was applied in patients with poor balance in
both the sitting and standing position. The early rehabilitation
team oriented the patient daily about his or her own data, time,
place and situation (reality orientation) to reduce confusion and
improve short-term memory as well as comprehension of their
surroundings.
Patients were shielded from too much light and sound. Visitors
were told to keep visits short and usually only one visitor at a time
was allowed. Patients were instructed to minimize TV watching
and reading, especially reading on a computer or smart phone
screens.
An informative brochure about aSAH was handed out to all
patients and their families. By explaining and discussing relevant
points from the brochure the patients and/or their families were
informed about typical symptoms and problems after aSAH and
received recommendations for further rehabilitation. The bro-
chure was also sent together with a discharge summary to the next
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Early rehabilitation after SAH 3
4 90), ICP 520, oxygen saturation (O2%) 495%, carbon dioxide
(CO2) pressure between 3.5 and 6, heart rate between 40 and 100,
and respiratory frequency 12–20. Clinical vasospasm and/or
severe multi-vessel vasospasm on computed tomography, digital
subtraction angiography and/or transcranial Doppler ultrasonog-
raphy gave rise to a pause or step back in mobilization, as
presented in Figure 1.
Clinical and outcome measures
Clinical and radiological features were collected from the patient
records. The rehabilitation needs were assumed to be related to
the patient’s clinical condition and especially to the presence of a
neurological deficit. In a systematic review of SAH grading scales
[25] the most important predictor of death and disability was level
of consciousness, whereas the most important predictor of
disability was hemiparesis and/or aphasia.
Therefore, we used the World Federation of Neurological
Surgeons (WFNS) grading scale [22] for assessing the clinical

grade. WFNS is based on the Glasgow Coma Scale (GCS) and

hospital and to the patient’s general practitioner.
acknowledges the presence of a major focal neurological deficit
(aphasia and/or hemiparesis or hemiplegia); Table 1. In WFNS
Mobilization algorithm
grade 1 the GCS is 15 and there is no motor deficit. In grade 2,
The main focus of early rehabilitation was passive and active there is a slight reduction in GCS to 14–13 but no motor deficit. In
mobilization to a sitting and standing position as early as possible, grade 3, the GCS is also 14–13 but there exists a motor deficit.
even if patients continued to require mechanical respiratory In grades 4 and 5, there may, or may not be a motor deficit, but
support or had a neurological deficit and/or impaired conscious-
ness. All patients received rehabilitation in the supine position
with head elevation at 30 from the first day after securing of the Table 1. The World Federation of Neurological Surgeons Scale.
aneurysm and thereafter in accordance with our stepwise
For personal use only.

mobilization algorithm as presented in Figure 1. An angle meter Major focal

was used to determine the degree of head elevation. Grade GCSa neurological deficitb
Progress in mobilization in aSAH patients was tailored I 15 
individually according to a mobilization algorithm, as presented II 14–13 
in Figure 1. With no deviation in the individually defined III 14–13 +
thresholds on surveillance parameters, no neurological deterior- IV 12–7 +/
V 6–3 +/
ation and no patient discomfort, mobilization was advanced.
Surveillance parameters in our SAH guidelines included limits for a
GCS: Glasgow Coma Score.
b
mean arterial pressure (MAP) 480, cerebral perfusion pressure Major focal neurological deficit (aphasia and/or hemiparesis or
(CPP) 470 (in the presence of vasospasm increased to up to CPP hemiplegia).

Figure1. Mobilization algorithm. *Severe vasospasms: go to step 0. Symptoms under mobilizing: go back to the step as tolerated. Acceptable
mobilization: ask the neurosurgeon if the next step is allowed. There will always be individual assessment.
 4 T. Karic et al. Disabil Rehabil, Early Online: 1–9

GCS is reduced from 12 to 7 in grade 4 and as low as 3–6 in grade
5 (Table 1).
To describe and quantify early rehabilitation, we registered the
time (in minutes) used on each of the early rehabilitation
categories daily for each patient. The PT also registered when
the mobilization step was changed.
Factors of feasibility were as follows: the number of days until
the initiation of early rehabilitation, the percent of patients not
available for early rehabilitation and the percent of patients who
could advance through our mobilization algorithm. We also
registered the occurrence of vasospasm and the frequency of
unintended removal of lines and tubes.
Data analysis and statistics
For analysis purposes, the patients were dichotomized into good-
grade (WFNS scores 1 and 2) and poor-grade (WFNS scores 3, 4
and 5) according to the WFNS at arrival at the NIW.
The data were not normally distributed. Continuous variables
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the aneurysm, however, none of these differences reached the
statistical significance.
The 30-day case fatality rate was 5.4% (one poor-grade and
one good-grade patient). In one case, the cause of death was
thrombosis of both posterior cerebral arteries (treated large basilar
tip aneurysm) 30 days after coiling of the aneurysm. In the other
patient, death occurred 27 days after ictus due to neurosurgical
and medical complications. The 30-day case fatality rate among
all aSAH patients treated in the same period was 17.8% (n ¼ 56,
including 19 patients who were never transferred to NIW and
therefore excluded in the present study).
Content of early rehabilitation
The rehabilitation content varied depending on the patient’s
clinical status (good grade versus poor grade) as shown in Table 3.
In total, the early rehabilitation team used significantly more time
per patient in the poor-grade group. The most time-consuming
component in both the groups was stimulation to activity and

are presented as the median and range, and the Mann–Whitney U
test was used to compare differences between the WFNS severity
groups. Categorical variables were presented by frequencies/
percentages, and the Chi-square test was used to compare
differences between the WFNS severity groups. A significance
level of 5% was adopted. The analyses were performed in SPSS v
18 (SPSS Inc., Chicago, IL).
body exercises followed by time used on mobilization. As
expected, positioning in neutral, passive exercises, assistance in
Table 3. The amount of total time (in minutes) used in each early
rehabilitation category, per patient, during our rehabilitation time in
good-grade (WFNS 1, 2) versus poor-grade (WFNS 3, 4, 5) patients
(median, range).

Good grade Poor grade

Results Early rehabilitation categories WFNS 1, 2 WFNS 3, 4, 5 p
Patients’ clinical characteristics Positioning 0 (0–185) 42 (0–130) 0.02
For personal use only.

Pulmonary rehabilitation 55 (0–180) 27 (0–90) NS

WFNS was a median of 2 (range 1–4) in the 37 included patients Passive exercises 0 (0–70) 17 (0–120) 0.01
when arrived at the NIW. The median age was 58 (35–74) years. Guidance in ADL 0 (0–45) 0 (0–130) 0.07
All the patients had their aneurysm secured within 34 h after Swallowing and eating 0 (0–40) 10 (0–85) 0.002
arrival to our hospital (median five hours). Approximately 11% of Mobilization 60 (0–135) 37 (0–150) NS
the patients required the insertion of a ventriculo-peritoneal shunt Activation 85 (0–240) 72 (0–185) NS
during the primary stay (27% received a shunt at any given point Balance training 0 (0–30) 0 (0–70) NS
Reality orientation 0 (0–75) 12 (0–35) NS
of time after aSAH).The characteristics of the good- and poor- Information 0 (0–95) 0 (0–60) NS
grade patients according to the WFNS scores are presented in Total rehabilitation time 240 (0–915) 412 (100–635) 0.04
Table 2. There was a higher fraction of females in the poor grade
patients, alongside with higher age and a shorter time to securing WFNS: World Federation of Neurological Surgeons scale.

Table 2. Clinical characteristics and management in patients with good versus poor clinical grade status according to the World Federation of
Neurological Surgeons (WFNS) scale at arrival to the neuro-intermediate ward (NIW).

Good grade Poor grade

(WFNS 1,2) (n ¼ 25) (WFNS 3,4,5) (n ¼ 12) p
Age (median, range) 56 (35–74) 62 (38–73) NS
Male/female (%) 36/64 17/83 NS
WFNS at arrival at the NIW WFNS1 ¼ 12; WFNS2 ¼ 13 WFNS3 ¼ 8; WFNS4 ¼ 4
aSAH treatment
Time to securing the aneurysm (hours) (median, range) 6.8 (0.5–34.4) 3.3 (0.6–14.4) NS
Surgical clip ligation/endovascular coil embolization (%) 32/68 50/50 NS
Patients with an intracranial pressure sensor (%) 64 92 0.07
Patients with an external ventricular drain (%) 60 92 0.05
Patients with lumbar drainage (%) 67 50 NS
Complications
Complications during the securing of the aneurysm (%)a 32 25 NS
Cerebral infarction visible on MRI (%) 32 33 NS
Pneumonia (%) 36 67 0.08
Length of treatment/stay
Days on mechanical ventilatory support (median, range) 0.9 (0–19.8) 8.9 (0–23) 0.06
Length of treatment in general intensive care (ICU) in days, 0.4 (0–19.5) 5.8 (0–19) 0.005
(median, range)
Length of treatment at NIW in days (median, range) 12 (1–36) 9 (3–33) NS
a
Complications during the securing of aneurysm: rebleeding before securing of the aneurysm, rupture or perforation of the aneurysm during coiling or
clipping, thromboembolism\vessel occlusion during coiling or clipping.
 DOI: 10.3109/09638288.2014.966162 Early rehabilitation after SAH 5
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Figure 2. Median time and standard deviation (in minutes) used by the early rehabilitation team per day in good grade(WFNS 1,2) versus poor grade
(WFNS 3,4,5) patients. WFNS: World Federation of Neurological Surgeons Scale.

eating and ADL were much more time-consuming in the poor-

grade group. Only 7 patients (28%) and/or their families in the
good-grade group and 3 (25%) in the poor-grade group received
information from the rehabilitation team with a huge range in
For personal use only.

minutes used on informative support (Table 3). Information was

also provided by the neurosurgeon, but time used and frequency
was not registered.
Most rehabilitation efforts were applied during the first seven
days at the NIW as presented in Figure 2. During the first week,
there was more time spent on poor grade patients, whereas this
difference evened out from Day 8 as illustrated in Figure 2.

Progress in mobilization and feasibility of early

rehabilitation
The progress in the mobilization steps (median) is presented in
Figure 3. More patients in the poor-grade group (16%) began with
mobilization at the ICU versus 4% of the good-grade patients.
Mobilization to 60 of head elevation in good-grade patients
started on the first day after securing the aneurysm (range 1–20),
and patients were mobilized to sitting in a chair (Out of Bed) on
the third day (range 3–24). Poor-grade patients started with
mobilization to 60 of head elevation on the third day after
securing the aneurysm (range 3–13) and were mobilized to out of
bed on the seventh day (range 7–25). The progress in mobilization
from step one (60 of head elevation) to step four (Out of Bed)
was significantly faster in the good-grade than in the poor-grade
group (p50.01). Nevertheless, the mobilization step at discharge
was a median of 6 (mobilized to walking) in both the groups.
Patients were discharged from our hospital when further
neurosurgical treatment was unnecessary, and they had obtained
different stages of mobilization at the point of discharge. Hence,
8% of poor-grade patients were discharged before they were
mobilized to sitting at the bedside, 25% before they were
mobilized out of bed (12% of good-grade patients), 42% before
mobilizing to standing (20% of good-grade patients) and 58%
before mobilizing to walking (32% of good-grade patients). No
patients (independent of step reached) had restrictions in further
mobilization at discharge, and further gradual mobilization was
recommended.
Figure 3. Median time (in days) to degree of mobilization according
to mobilization algorithm. Dichotomization of data in relation to the
clinical status (good versus poor grade) according to World Federation of
Neurological Surgeons score.
Fifteen of 37 patients required a cessation or reduction in
mobilization, eight of them due to diagnosed moderate or severe
cerebral vasospasm (seven in the good-grade and one in the poor-
grade group). Steps back due to vasospasm occurred from day 6 to
day 16 after securing the aneurysm (median 8 days). Further
mobilization after pausing due to vasospasms occurred after a
median of 5 days (range 2–11). In the other patients, break in
mobilization was caused by headache (2 patients), fatigue
(1 patient), hypertension and tachycardia above the individually
recommended thresholds (2 patients), and hydrocephalus
(2 patients). Three patients (8%), all in the good-grade group,
developed mild vasospasm and were in accordance with the
algorithm mobilized further without any problems. One patient
had a step back due to an atypical development of symptoms.
Mobilization was complicated by neurological deterioration on
day 10, after mobilization to standing bedside. The treating
neurosurgeons agreed on the origin of the patient’s symptoms
being thromboembolic and aggravated by Nimodipine treatment
of vasospasm. Further mobilization was continued according to
the mobilization algorithm.
 6 T. Karic et al.
Discussion
In the present study, we described and quantified the content of
early rehabilitation developed for patients with aSAH and deemed
it feasible from day one after securing of the aneurysm.
Clinical characteristics and choice of group affiliation
We had no upper age limit for the patients in the present study. As
long as an elderly patient was deemed suited for ruptured
aneurysm securing, we also considered this patient as suitable for
early rehabilitation. Moreover, experience from previous studies
indicated no direct correlation between age and outcomes after
treatment of aSAH [24] and stroke [26].
The lower age of 18 was chosen due to several reasons: it is the
lower age limit due to the Ethical regulations in Norway and
patients below 18 were treated in pediatric units. Most import-
antly, pediatric aSAH represents a different pathophysiological
entity as compared to adult aSAH [27].
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Patients with aSAH are typically graded in categories of
‘‘good’’ and ‘‘poor’’ grade in accordance with their clinical
condition prior to securing the aneurysm. In addition to a
neurological deficit caused by aSAH, a neurological deficit may
be acquired during or after securing the aneurysm. As neuro-
logical deficits affect the content of rehabilitation, we chose the
WFNS categorization at arrival at the NIW to provide the most
precise estimate of rehabilitation needs.
Not surprisingly, a larger percentage of poor-grade patients had
received surgical clip ligation of the aneurysm, usually due to the
presence of intracerebral hemorrhage. Clip-ligated patients were
For personal use only.
also more likely to present with a major motor neurological
deficit and hence were affiliated with the poor-grade WFNS
group. Poor-grade patients also required more frequent ICP
monitoring and had more hydrocephalus problems in addition to a
higher frequency of pulmonary infections. These characteristics
could influence the content of rehabilitation because symptoms
with respect to post-surgical pain required a higher degree of
caution in mobilization and more extensive monitoring kept them
bed-ridden for a longer time.
Content of early rehabilitation
The preservation of vital functions after aSAH and securing of the
aneurysm follows standardized protocols [1], but rehabilitation is
more controversial. In general, the content and amount of
neurorehabilitation is often poorly described [17,20,28], and the
time to the initiation of early rehabilitation varies widely. Hence,
different studies about early rehabilitation after TBI reported the
following times of initiation of rehabilitation: median of 12 d
(IQR 8) after injury in the study of Andelic et al. [12]; average of
19.6 d in the study of Engberg et al. [24]; 27 d (range 3–126) in
the study of Sandhaug et al. [29] and 30 d after injury in the study
of Sorbo et al. [13]. In stroke rehabilitation, mobilization often
starts earlier, typically on the second day after admission to the
hospital [26]. Olkowski et al. [30] described an early mobilization
program for aSAH patients that were initiated 3.2 d (SD 1.3) after
aSAH, and the authors applied predetermined criteria for
participation in the protocol. In the present study, rehabilitation
started immediately after transfer to the NIW, generally within the
first day after ictus. Longer stay in the ICU for poor-grade patients
was the reason for the later initiation of early rehabilitation in this
group. Possibly, this group may profit from an even earlier
initiation of rehabilitation similar to patients after TBI as
published in the study of Andelic et al. [12].
Titsworth et al. [31] emphasized that due to the risk of
vasospasms, SAH patients require a much higher degree of
invasive surveillance than stroke and TBI patients, including those
Disabil Rehabil, Early Online: 1–9
without neurological and cognitive deficit. This is one of the
reasons that early rehabilitation experience from other neurosur-
gical patients could not be directly applied in aSAH patients.
However, the amount of rehabilitation during the first seven
days in the present study is comparable with the amount used
in early mobilization protocols after stroke [26]. The amount of
rehabilitation after moderate and severe TBI described in the
study of Sandhaug et al. [29] was larger (2–3 h), most likely
because more than 70% of the patients with moderate and severe
TBI also sustain other traumatic injuries [32].
Because aSAH patients exhibited increased fatigability,
impaired learning ability and short-term memory, short sessions
and frequent repetitions were necessary. Similarly, better results
were achieved in stroke patients receiving rehabilitation in more
frequent but shorter sessions compared with patients receiving the
same dose in longer sessions [26].
The clinical status was decisive for the amount and content of
early rehabilitation. Pulmonary rehabilitation was applied fre-
quently in both groups, but the median was actually lower in the
poor-grade patients, most likely because the poor-grade patients
arrived at the NIW at a later point of time during the course after
SAH, and their most serious pulmonary problems may have been
cured already at the ICU. This finding emphasizes the need for
early pulmonary rehabilitation in all patients regardless of the
severity of aSAH [31].
Positioning in neutral, exercises for contracture prevention,
guiding in activities of daily living (ADL) and assessment of
swallowing and eating were presently almost exclusively used in
patients with neurological deficits (WFNS 3,4,5). Hence, the
content of early rehabilitation in the poor-grade group was similar
to the rehabilitation content after severe TBI [12].
Reality orientation of our patients was initiated within 24 h
after admittance to the NIW. This scarcely time-consuming cat-
egory is an important component of early rehabilitation because
aSAH influences cognitive functions markedly [8].
The median time used on information and emotional support
to patients and their families was spread over few patients,
relatively short and similar across clinical conditions. The
standard information set-up and use of an informative brochure
was time saving. It is worth noting that information and support
given by the neurosurgeon was not scored because it was often
given outside of our registration period. Furthermore, some of the
families’ needs for information and emotional support may have
been satisfied immediately after the ictus during the phase of
treatment at the ICU.
However, the huge range in minutes used on informative
support reflect that some patients and/or families requested much
more information and emotional support through conversations
than the rest of the patients. The rehabilitation team was available
through regular working hours, and during that time, there was no
problem to include more thorough information alongside the rest
of the rehabilitation program. Research regarding the acute phase
after TBI has shown that the majority of relatives had severely
impaired quality of life and symptoms of anxiety and depression
at the time of admission [33]. Our study was not designed to give
an answer on that question and future research should focus
on developing and evaluating interventions for relatives in the
acute phase.
The volume of balance training was small in both groups, and
a probable explanation could be that not all of the patients were
maximally mobilized during the registration period.
A precise definition of the content of rehabilitation and its dose
is essential for advancing the science of treatment efficacy and
would improve communication across rehabilitation disciplines
[34–38]. We hope that description of our work can contribute to
knowledge sharing between professionals and institutions. It is,
 DOI: 10.3109/09638288.2014.966162
however, challenging to define parameters that can be used to
describe and quantify early rehabilitation more precisely. Well-
defined parameters are a prerequisite for a standardized protocol
for the comparison of rehabilitation interventions in the clinical
care of aSAH. Nevertheless, our study is one of the few in this
field, and further studies on the description of content, dose and
time to early rehabilitation are required and should eventually lead
to the standardization of early rehabilitation in aSAH.
Progress in mobilization and feasibility of early rehabili-
tation in aSAH patients
Mobilization is an inevitable part of early rehabilitation that
has proven to be effective for other acute neurological conditions
[10–17]. Although the head and body position is an important
element of intensive care and early rehabilitation, guidelines for
the management of aSAH do not include recommendations for
the degree of head elevation [1]. According to the guidelines, the
position of the head of the bed in sequence from 0 to 45 is
Disabil Rehabil Downloaded from informahealthcare.com by McMaster University on 02/27/15
believed to be safe [21], and ICP and CPP are not negatively
affected by passive and active movements with head elevation in
the 30 and 45 head-up position [39,40].
In stroke patients, the risk of increasing penumbra is a major
concern when performing early mobilization, whereas in aSAH
patients, a fear for exacerbation of cerebral vasospasm due to
early rehabilitation is eminent. After ischemic stroke, the time to
mobilization out of bed varies from 24 h to 6 d [17,26,28,41]. This
is comparable with our findings in aSAH patients, who could be
mobilized to the edge of the bed within 3 d after securing the
aneurysm and out of bed within 4 d, without observing adverse
For personal use only.
effects on the ICP or CPP. Although good-grade patients were
more likely to advance through the mobilization algorithm faster,
there was no statistically significant difference between the groups
with respect to the mobilization level at discharge. This obser-
vation is biased by the longer length of stay for poor-grade
patients and thus a higher chance to be mobilized to a higher
level. Not all the patients were hospitalized long enough to be
mobilized to walking. This explains the lower median for time
needed to reach mobilizing to walking than to standing for poor-
grade patients.
Although aSAH patients exhibit a more excessive grade of
invasive monitoring, we have not registered any correlation
between early rehabilitation and the percentage of unintended
removal of lines and tubes. Even the presence of an EVD or
lumbar drain did not represent any obstacle to mobilization.
One of our patients acquired new neurological deficits at the
mobilization level of standing. We cannot explain his deterior-
ation by either mobilization or cerebral vasospasm per se. The
most probable cause was a combined effect of moderate vaso-
spasm, low blood pressure during general anesthesia and
thromboembolism. His cerebral infarction may also have been
caused by the use of Nimodipine, as suggested by a similar case
report [42].
With respect to cerebral vasospasm, the experience in the
rehabilitation of TBI patients was that early rehabilitation did not
exacerbate vasospasm in patients with traumatic SAH [12];
however, we were aware that the risk of vasospasm may differ
between aSAH and traumatic SAH. In the present study, patients
with mild vasospasm could be mobilized further without adverse
effects. According to our mobilization algorithm, patients with
severe vasospasm returned to step 1, and further mobilization was
halted until the vasospasm resolved. In contrast to studies of
Titsworth et al. [31] and Olkowski et al. [30], we did not pre-
exclude patients who did not meet predefined clinical thresholds.
Our approach was to include all patients and rather to adjust the
rehabilitation individually according to the patient’s clinical status
Early rehabilitation after SAH 7
and then quantify and describe content. The frequency of cerebral
vasospasm in our patients was as expected and occurred within
the expected time frame of a median peak at day 8 and a duration
of 5 d. This concurs well with the reported maximal arterial
narrowing at 5 to 14 days and gradual resolution over 2 to 4 weeks
[43]. The higher frequency of vasospasms in the good-grade
patients can be explained by the fact that the poor-grade patients
most likely went through the phase with vasospasms at the ICU,
i.e. prior to arrival at the NIW. There is hence so far no indication
that early rehabilitation facilitates the development of cerebral
vasospasm. The number of patients in the present study, however,
is too small to draw final conclusions on the relationship of early
rehabilitation to cerebral vasospasm in aSAH, but this important
question will be addressed further in an ongoing study at our
department.
Early rehabilitation was tailored individually and was applied
in all patients from day one after transfer to NIW with head
elevation at 30 . The initiation of mobilization to 60 of head
elevation so soon (from 24 h) after securing the aneurysm, the
gradual increase of the mobilization degree during our treatment
time, and no restrictions in further mobilization after discharge
are indicators that early rehabilitation applying our mobilization
algorithm is feasible. This notion is supported by the relatively
low incidence of step back due to reasons other than vasospasm.
This corroborates the findings of Olkowski et al. [30], who in a
retrospective study of early mobilization after aSAH could not
identify an increased rate of complications.
To our knowledge, there are no randomized control trials
providing evidence for how long it is necessary to stay in bed
after aSAH, and we invite to international collaboration regarding
that issue.
Strengths and limitations
A measurement of environmental factors that affect rehabilitation
was not performed. The registration of early rehabilitation dose of
all early rehabilitation components was limited to working hours
of the interdisciplinary team and did not include activities that
patients had undertaken independently or with the help of nurses
outside of our recording time (08:00 a.m. to 03:00 p.m., 5 d per
week). It was assumed that the latter impact was evenly and
affected all patients equally. In addition, nurses followed-up the
recommendations of the rehabilitation team that was defined
during the day and decision of further mobilization was always
done with the whole interdisciplinary team during the daytime.
Furthermore, variations in the patient’s cultural background,
attitudes and comorbidities may interfere with the frequency of
used components.
We excluded patients with previous aSAH, brain injury or
neurodegenerative disorders that interfered with the assessment of
acute aSAH-related disabilities. Our experience suggests that
early rehabilitation principles and mobilization algorithm may
also be used in these patients as well as in patients with non-
aneurysmal SAH.
We acknowledge the limitations of a small sample size.
However, this study is merely a description of the content and
feasibility of early rehabilitation, whereas its effect on short- and
long-term outcomes will be evaluated in a larger, ongoing study.
Strength of the present study is that the early rehabilitation
team managed to motivate the clinical staff at the neurosurgi-
cal department to be part of our team and to continue the
rehabilitation goals in the afternoons and weekends. Thereby,
there was loyalty to the mobilization algorithm, resulting in a
standardized and rigorous protocol. Importantly, early rehabilita-
tion did not interfere with the performance of usual acute therapy,
even in poor-grade patients. Hence, our early rehabilitation
 8 T. Karic et al.
model can be implemented as a standard component into
neurointensive care.
Another advantage is that the study was conducted prospect-
ively and is thus, to the best of our knowledge, the first
prospective study to describe and quantify the content of early
rehabilitation in aSAH patients.
We attempt to ensure that patients receive continuous follow-
up after discharge from our department and will evaluate the
effect of early rehabilitation on complications, length of primary
stay and functional and cognitive outcome in a follow-up study.
Conclusions
Early rehabilitation in aSAH patients was feasible and could be
implemented from day one after securing the aneurysm under
careful monitoring of the clinical status. The content of early
rehabilitation varied according to the patient’s clinical condition
after securing of the aneurysm. Interdisciplinary collaboration is
recommended because of a need for close monitoring and
Disabil Rehabil Downloaded from informahealthcare.com by McMaster University on 02/27/15
adjustment of rehabilitation in the individual patient. However,
further research with a focus on the content, timing and intensity
of early rehabilitation in aSAH patients is recommended.
Acknowledgements
We would like to acknowledge the support of the clinical staff
at the neurosurgical department at Oslo University Hospital,
Rikshospitalet who worked with early rehabilitation compo-
nents required for this study. Special thanks are given to Ludvig
Toftedahl (physiotherapist) and Malin Mongs (occupational
For personal use only.
therapist), who performed early rehabilitation and collected
data. Without their hard work and the neurosurgeons’ supervision
carried out by the head of cerebrovascular surgery, Dr Wilhelm
Sorteberg, it would not have been possible to conduct this study.
Declaration of interest
The authors report no conflicts of interest with respect to the
research and authorship. The authors alone are responsible for the
content and writing of this article.
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