http://informahealthcare.com/dre ISSN 0963-8288 print/ISSN 1464-5165 online 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

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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, 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 adapted to patients with acute aneurysmal subarachnoid hemorrhage (aSAH) and to assess its feasibility. Methods: This was a prospective, observational study including 37 aSAH patients. 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 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 more rehabilitation (median 412 min) than did good-grade patients (WFNS 1, 2) (median 240 min). Mobilization to 60 of head elevation in good-grade patients began on day one after securing the aneurysm. Out-of-bed mobilization was possible on day three. Poorgrade 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.

Brain injury, early rehabilitation, intracranial aneurysm, mobilization, stroke, subarachnoid hemorrhage History Received 25 January 2014 Revised 1 August 2014 Accepted 12 September 2014 Published online 29 September 2014

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 Aneurysmal subarachnoid hemorrhage (aSAH) is a life-threatening condition accounting for approximately 3–5% of all strokes, with half of the patients being younger than 55 years [1,2]. The incidence rate ranges from 4 to 10 per 100 000 person-years in most countries. In Norway, the incidence rate of aSAH is approximately 10.0 per 100 000 person-years [3]. Early securing of the aneurysm, more aggressive drainage of cerebrospinal fluid (CSF) and improved neurointensive care have resulted in better survival rates [4,5], but the case fatality remains high. In the last three decades, the case fatality rate for aSAH in Norway at 1, 3, 7 and 30 days was 14%, 20%, 24% and 36%, respectively [6]. Cerebral ischemia is considered a crucial risk factor for poorer neurological outcome and increased case fatality [7]. After the early securing of the aneurysm, intensive care Address for correspondence: Dr Tanja Karic, Department of Physical Medicine and Rehabilitation, Oslo University Hospital, Ullevaal, P.B. 4950 Nydalen, Oslo 0424, Norway. E-mail: [email protected]

management of patients with aSAH focuses on the reduction of secondary brain damage and the prevention of further neurological injury. Aneurysmal rebleeding, hydrocephalus, cerebral vasospasm and seizures represent the most severe secondary complications [1]. Pneumonia, meningitis, electrolyte abnormalities and thrombosis represent common medical complications [1]. Together with critical illness myeloneuropathy, these complications contribute to the burden of care in the acute phase. Long-term problems in survivors of aSAH include physical, emotional and cognitive difficulties, contributing to limitations in activities and participation in social activities and work [8,9]. In non-SAH stroke care and traumatic brain injury (TBI) care, early rehabilitation has been established as an integral part of acute and sub-acute treatment, resulting in reduced mortality, fewer complications and better functional outcomes [10–17]. Current recommendations in rehabilitation after acute ischemic stroke include mobilization out of bed as early as possible [18]. However, there remains a need for a consensus on what type of rehabilitation with what content and dose should be implemented early in different patients groups [19,20]. Thus, early

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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 potentially 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 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. 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 transferred 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),

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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 interdisciplinary approach [23] and consisted of a rehabilitation physician, a neurosurgeon, a physical therapist (PT), an occupational therapist (OT) and nurses with special expertise within the care of vascular neurosurgical patients. A clinical neuropsychologist, speech therapist and medical social workers were also available. The entire early rehabilitation team defined rehabilitation 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 recommendations 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 inspiration for our early rehabilitation program but needed modification 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 complications. 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.

Early rehabilitation after SAH

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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 brochure was also sent together with a discharge summary to the next hospital and to the patient’s general practitioner. Mobilization algorithm The main focus of early rehabilitation was passive and active mobilization to a sitting and standing position as early as possible, even if patients continued to require mechanical respiratory support or had a neurological deficit and/or impaired consciousness. All patients received rehabilitation in the supine position with head elevation at 30 from the first day after securing of the aneurysm and thereafter in accordance with our stepwise mobilization algorithm as presented in Figure 1. An angle meter was used to determine the degree of head elevation. Progress in mobilization in aSAH patients was tailored individually according to a mobilization algorithm, as presented in Figure 1. With no deviation in the individually defined thresholds on surveillance parameters, no neurological deterioration and no patient discomfort, mobilization was advanced. Surveillance parameters in our SAH guidelines included limits for mean arterial pressure (MAP) 480, cerebral perfusion pressure (CPP) 470 (in the presence of vasospasm increased to up to CPP

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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 ultrasonography 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 acknowledges the presence of a major focal neurological deficit (aphasia and/or hemiparesis or hemiplegia); Table 1. In WFNS grade 1 the GCS is 15 and there is no motor deficit. In grade 2, there is a slight reduction in GCS to 14–13 but no motor deficit. In grade 3, the GCS is also 14–13 but there exists a motor deficit. In grades 4 and 5, there may, or may not be a motor deficit, but Table 1. The World Federation of Neurological Surgeons Scale.

Grade

GCSa

Major focal neurological deficitb

I II III IV V

15 14–13 14–13 12–7 6–3

  + +/ +/

a

GCS: Glasgow Coma Score. Major focal neurological deficit (aphasia and/or hemiparesis or hemiplegia).

b

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.

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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.

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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

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Data analysis and statistics

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 body exercises followed by time used on mobilization. As expected, positioning in neutral, passive exercises, assistance in

For analysis purposes, the patients were dichotomized into goodgrade (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 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).

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).

Results

Early rehabilitation categories

Good grade WFNS 1, 2

Poor grade WFNS 3, 4, 5

Patients’ clinical characteristics

Positioning Pulmonary rehabilitation Passive exercises Guidance in ADL Swallowing and eating Mobilization Activation Balance training Reality orientation Information Total rehabilitation time

0 55 0 0 0 60 85 0 0 0 240

42 27 17 0 10 37 72 0 12 0 412

WFNS was a median of 2 (range 1–4) in the 37 included patients when arrived at the NIW. The median age was 58 (35–74) years. All the patients had their aneurysm secured within 34 h after arrival to our hospital (median five hours). Approximately 11% of the patients required the insertion of a ventriculo-peritoneal shunt during the primary stay (27% received a shunt at any given point of time after aSAH).The characteristics of the good- and poorgrade patients according to the WFNS scores are presented in Table 2. There was a higher fraction of females in the poor grade patients, alongside with higher age and a shorter time to securing

(0–185) (0–180) (0–70) (0–45) (0–40) (0–135) (0–240) (0–30) (0–75) (0–95) (0–915)

(0–130) (0–90) (0–120) (0–130) (0–85) (0–150) (0–185) (0–70) (0–35) (0–60) (100–635)

p 0.02 NS 0.01 0.07 0.002 NS NS NS NS NS 0.04

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).

Age (median, range) Male/female (%) WFNS at arrival at the NIW aSAH treatment Time to securing the aneurysm (hours) (median, range) Surgical clip ligation/endovascular coil embolization (%) Patients with an intracranial pressure sensor (%) Patients with an external ventricular drain (%) Patients with lumbar drainage (%) Complications Complications during the securing of the aneurysm (%)a Cerebral infarction visible on MRI (%) Pneumonia (%) Length of treatment/stay Days on mechanical ventilatory support (median, range) Length of treatment in general intensive care (ICU) in days, (median, range) Length of treatment at NIW in days (median, range) a

Good grade (WFNS 1,2) (n ¼ 25)

Poor grade (WFNS 3,4,5) (n ¼ 12)

56 (35–74) 36/64 WFNS1 ¼ 12; WFNS2 ¼ 13

62 (38–73) 17/83 WFNS3 ¼ 8; WFNS4 ¼ 4

NS NS

6.8 (0.5–34.4) 32/68 64 60 67

3.3 (0.6–14.4) 50/50 92 92 50

NS NS 0.07 0.05 NS

32 32 36

25 33 67

NS NS 0.08

0.9 (0–19.8) 0.4 (0–19.5) 12 (1–36)

8.9 (0–23) 5.8 (0–19) 9 (3–33)

p

0.06 0.005 NS

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.

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DOI: 10.3109/09638288.2014.966162

Early rehabilitation after SAH

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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 poorgrade 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 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 poorgrade 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.

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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.

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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 importantly, pediatric aSAH represents a different pathophysiological entity as compared to adult aSAH [27]. 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 neurological 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 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

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without neurological and cognitive deficit. This is one of the reasons that early rehabilitation experience from other neurosurgical 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 frequently 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 category 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,

Early rehabilitation after SAH

DOI: 10.3109/09638288.2014.966162

however, challenging to define parameters that can be used to describe and quantify early rehabilitation more precisely. Welldefined 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.

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Progress in mobilization and feasibility of early rehabilitation 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 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 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 observation 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 poorgrade 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 deterioration by either mobilization or cerebral vasospasm per se. The most probable cause was a combined effect of moderate vasospasm, 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 preexclude 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

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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 nonaneurysmal 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 neurosurgical 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 rehabilitation did not interfere with the performance of usual acute therapy, even in poor-grade patients. Hence, our early rehabilitation

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T. Karic et al.

model can be implemented as a standard component into neurointensive care. Another advantage is that the study was conducted prospectively 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 followup 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.

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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 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 components required for this study. Special thanks are given to Ludvig Toftedahl (physiotherapist) and Malin Mongs (occupational 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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