http://informahealthcare.com/idt ISSN 1748-3107 print/ISSN 1748-3115 online Disabil Rehabil Assist Technol, Early Online: 1–6 ! 2014 Informa UK Ltd. DOI: 10.3109/17483107.2014.908246

RESEARCH PAPER

Work-rate-guided exercise testing in patients with incomplete spinal cord injury using a robotics-assisted tilt-table Disabil Rehabil Assist Technol Downloaded from informahealthcare.com by Michigan University on 10/11/14 For personal use only.

Marco Laubacher1, Claudio Perret2, and Kenneth J. Hunt1 1

Division of Mechanical Engineering, Department of Engineering and Information Technology, Institute for Rehabilitation and Performance Technology, Bern University of Applied Sciences, Burgdorf, Switzerland, and 2Institute of Sports Medicine, Swiss Paraplegic Centre, Nottwil, Switzerland Abstract

Keywords

Purpose: Robotics-assisted tilt-table (RTT) technology allows neurological rehabilitation therapy to be started early thus alleviating some secondary complications of prolonged bed rest. This study assessed the feasibility of a novel work-rate-guided RTT approach for cardiopulmonary training and assessment in patients with incomplete spinal cord injury (iSCI). Methods: Three representative subjects with iSCI at three distinct stages of primary rehabilitation completed an incremental exercise test (IET) and a constant load test (CLT) on a RTT augmented with integrated leg-force and position measurement and visual work rate feedback. Feasibility assessment focused on: (i) implementation, (ii) limited efficacy testing, (iii) acceptability. Results: (i) All subjects were able follow the work rate target profile by adapting their volitional leg effort. (ii) During the IETs, peak oxygen uptake above rest was 304, 467 and 1378 ml/min and peak heart rate (HR) was 46, 32 and 65 beats/min above rest (subjects A, B and C, respectively). During the CLTs, steady-state oxygen uptake increased by 42%, 38% and 162% and HR by 12%, 20% and 29%. (iii) All exercise tests were tolerated well. Conclusion: The novel work-rate guided RTT intervention is deemed feasible for cardiopulmonary training and assessment in patients with iSCI: substantial cardiopulmonary responses were observed and the approach was found to be tolerable and implementable.

Cardiopulmonary exercise testing, incomplete spinal cord injury, rehabilitation, robotics-assisted tilt-table History Received 4 November 2013 Revised 17 February 2014 Accepted 21 March 2014 Published online 8 April 2014

ä Implications for Rehabilitation   

Work-rate guided robotics-assisted tilt-table technology is deemed feasible for cardiopulmonary assessment and training in patients with incomplete spinal cord injury. Robotics-assisted tilt-tables might be a good way to start with an active rehabilitation as early as possible after a spinal cord injury. During training with robotics-assisted devices the active participation of the patients is crucial to strain the cardiopulmonary system and hence gain from the training.

Introduction Following a spinal cord injury, a stroke or some other neurological impairment, it is important to initiate the rehabilitation process as early as possible to alleviate the manifold secondary complications of prolonged bed rest; rapid cardiovascular deconditioning is one important consequence of immobility, muscle weakness and neuro-degeneration are others [1]. Besides these complications, the restricted cardiovascular capacity can also affect the daily exercise routine and therefore limit the patient’s recovery [2,3].

Address for correspondence: Marco Laubacher, Division of Mechanical Engineering, Department of Engineering and Information Technology, Institute for Rehabilitation and Performance Technology, Bern University of Applied Sciences, CH-3400 Burgdorf, Pestalozzistrasse 20, 3400 Burgdorf, Switzerland. Tel: 0041 34 426 41 96. E-mail: marco. [email protected]

There are different strategies for early activation of the cardiovascular system. Here, we briefly review the literature regarding: (i) passive cyclical limb movement, (ii) tilt-table therapy and (iii) robotics-assisted tilt-table (RTT) technology. Passive cyclical limb movement has been shown to increase heart stroke volume (SV) and cardiac output in spinal cord injured subjects [4]. In healthy subjects, passive cyclical limb movement also initiates an increase of the heart rate (HR) [5]. The use of a tilt-table was shown to be important for prevention of several secondary complications such as decubitus ulcers and spasticity but also for improvement of pulmonary ventilation [6–9]. However, a common problem of head-up tilt during primary rehabilitation is the occurrence of syncope [10,11]. The addition of passive limb movement gave a more stable blood pressure and absence of any signs of syncope and loss of consciousness, which underlines the influence of leg movements to stabilize the cardiovascular system [12,13]. However, the intensity during passive mobilisation is not sufficient to increase cardiopulmonary fitness [14]. Therefore, the active participation of the subjects

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Table 1. Subject characteristics.

Subject A B C

Age

Body mass

Time since injury

Lesion level and grade

38 52 19

80.1 kg 73.3 kg 71.5 kg

4 mth 5 mth 3 mth

T12, AIS C L3, AIS C L1, AIS D

Rehabilitation status Lokomat training Parallel bar training Supported walking training

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Mth, months; T, thoracic; L, lumbar; AIS, American Spinal Injuries Association Impairment Scale.

is required. Enhanced muscle activity increases the ventilatory _ 2 ), the heart rate (HR) [15] and leads to higher oxygen uptake (VO cortical activation in gait-related brain regions [16]. Active participation evokes further benefits including better motor performance resulting from more stable motor patterns in the brain [17,18]. A novel work-rate-guided RTT approach was recently proposed based on functional extension of a commercial RTT [19]. This supports patients’ active participation in the exercise using a biofeedback system: the system employs leg-force and position measurement sensors, and a screen which shows target and actual work rates. This type of feedback generally enhances motivation [20,21] and stimulates motor and sensory skills [22,23], but it remains to explore the potential of work-rate guided RTT for cardiopulmonary rehabilitation. The aim of the present study was to assess the feasibility of the work-rate-guided RTT intervention [19] for cardiopulmonary training and assessment in a small but representative sample of subjects with incomplete spinal cord injury (iSCI) at three distinct stages of primary rehabilitation. Feasibility assessment focused on implementation, limited efficacy testing and acceptability, with a view to deciding whether further efficacy testing of the work-rate guided RTT approach is warranted.

Methods Subjects This feasibility study was carried out at the Institute of Sports Medicine at the Swiss Paraplegic Centre in Nottwil. Patients were screened by the responsible medical scientist for possible inclusion. Inclusion criteria were: traumatic iSCI below level T6 (to exclude the possibility of autonomic dysreflexia or disrupted sympathetic exercise responses), being in primary rehabilitation, medically stable and physically resilient. Each subject had to be at a different stage of the rehabilitation process as detailed below. Exclusion criteria included cardiopulmonary contraindications, any history of autonomic dysreflexia, osteoporosis, decubitus ulcers, significant restrictions in range of motion, talipes equinus, acute periarticular ossification and current fractures. Three subjects were recruited (Table 1). Subject A showed the weakest activity in the lower extremities. In his regular rehabilitation programme, this subject had recently started with passive Lokomat1 training. Subject B had just started with parallel bar training and subject C had started with supported overground walking training. The study was reviewed and approved by the Ethics Committee of the Swiss Canton of Lucerne and all subjects provided written informed consent prior to participation.

1

Lokomat: motor driven gait orthosis (Hocoma AG, Volketswil, Switzerland).

Figure 1. The modified Erigo tilt-table with the feedback screen in front of the subject and the force measurement sensors visible at the leg brace.

Instruments We utilised a RTT (Erigo, Hocoma AG, Volketswil, Switzerland), upgraded with force measurement sensors (Transmetra haltec GmbH, Schlattingen, Switzerland) and a visual feedback system [19]. The force sensors are load cells with a range up to 500 N and a measurement precision of 0.1%. Using the step frequency, the angular velocity and the lever arm of the force, the total mechanical work rate Ptotal was calculated in real time. To calculate the active mechanical work (Pmech) produced by the subject’s volitional effort, the initially measured passive work rate (i.e. the work rate necessary for movement of the subject’s legs by the drives) was subtracted from Ptotal. Pmech was smoothed by a first order IIR low-pass filter with a cut-off frequency of 0.02 Hz and projected onto a screen directly visible to the subject together with the target mechanical work rate Pmech. Target mechanical work rate was adapted to the subject’s motor abilities observed during the first part of the test. Subjects were instructed to maintain this target work rate as closely as possible by applying force via the thigh cuffs in the direction of movement (Figure 1). Pulmonary gas exchange was measured breath-by-breath by open spirometry (Metamax 3B, Cortex Biophysik GmbH, Germany). The device was calibrated prior to each test using a volumetric syringe and precision gas mixture in accordance with the manufacturer’s recommendations. HR was measured by a HR belt (T31, Polar Electro, Kempele, Finland) and recorded via telemetry on the Metamax 3B system and also using a separate receiver (HRMI, Sparkfun, Boulder, CO) for higher resolution. Blood pressure was measured prior to the test and every 3 min

Exercise testing with iSCI subjects using RTT

DOI: 10.3109/17483107.2014.908246

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Table 2. Rest measurement parameters (mean ± SD) obtained during the last 2 min of the rest measurement phase in a supine position. Subject A B C

HR [beats/min]

_ 2 [ml/min] VO

_ VCO 2 [m/min]

91 (±2.2) 62 (±2.4) 88 (±2)

302 (±13.7) 352 (±23) 488 (±10.6)

226 (±9.8) 226 (±16) 346 (±7.2)

_ _ 2 , oxygen uptake volume; VCO HR, heart rate; VO 2 , expired carbon dioxide volume.

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Outcome measures and analysis

Figure 2. A schematic representation of (a) the incremental exercise test (IET) and (b) the constant load test (CLT). The solid line represents the target mechanical work rate (Pmech ), which was presented on the screen in front of the subjects. Both tests last 20 min and started with a 5-min passive phase, followed by an active phase. The duration of the active phase was exactly 10 min in the CLT. IET duration depended on the subject’s performance and the termination criteria, but was limited to 10 min. A second passive phase followed.

during the test using a sphygmomanometer (HEM-907, Omron Corporation, Kyoto, Japan).

Feasibility assessment focused on: (i) implementation (were the subjects able to follow the visual work rate target?), (ii) limited efficacy testing (was there a measurable cardiopulmonary reaction?), (iii) acceptability (was the exercise tolerable?). The following parameters were estimated from the IET for _ 2 peak ), peak heart efficacy testing (ii): peak oxygen uptake (VO rate (HRpeak), gas exchange threshold (GET), peak work rate (Pmpeak ), and oxygen uptake and HR kinetics. The CLT outcomes _ 2 , HR and contributing to efficacy testing were delta values for VO mechanical work rate (DPmech ) and the time constants of oxygen uptake kinetics and HR. The respiratory values were smoothed with a 15-breath moving average filter [24] and were used for estimation of respiratory peak values. The time constants and HR values were calculated using unfiltered data. Pmech was smoothed by a first-order IIR low-pass filter with a 20-mHz bandwidth. For calculation of delta values, the means of the final 2 min of each performance level were used. Additionally, after each test subjects rated their perceived exertion according to the CR-10 Borg scale for RPE [25]. Acceptability criterion (iii) was assessed by oral questioning of the subjects and physiotherapists. What is your personal feedback on the task? How challenging and how comfortable was it? Would you want to train on this device?

Results Procedures Subjects were accompanied during each test by their physiotherapist who assisted with subject transfer and handling. Each test comprised one session of about 120 min separated into three phases. In the first phase, subjects were introduced to the test setup and specific adjustments were carried out. Subjects were tilted to 60 and the legs were passively moved at 40 steps per minute (spm) by the leg drives to measure the passive forces. Then they completed an exercise task at 60 to familiarize themselves with the test environment and, if necessary, adjustments to the tilt-table setup were carried out. If so, a second passive measurement was conducted. The exercise familiarization was followed by a resting measurement in the supine position. In the second phase the subjects were tilted to 60 and performed an incremental exercise test (IET) (Figure 2a). The test was terminated by the investigator if one of the following conditions occurred: (1) pain, (2) decreasing movement quality, (3) target performance was not reached for more than 20 s. The subjects were then moved passively for another 5 min. The second phase was followed by a short rest period of about 10 min and, after recovery, the third phase started. In this phase a constant load test (CLT) (Figure 2b) was performed at a level of at least 40% of the previously reached maximum work rate. In order to load the cardiovascular system of the subjects to an adequate level, the performance level of the CLT could be increased up to 60% of maximum if coordinative deficits seemed to have limited the maximum performance during the IET.

Implementation (i): All three subjects were able to apply force on the leg braces and to interpret the visual feedback. The slope of the IET was adapted to the individual motor abilities observed during familiarisation so that the maximum work rate would be reached in the optimal timeframe of approximately 10 min: 1.5 W/min for subject A, 3 W/min for subject B and 4 W/min for subject C. Target work rate for the CLT was set in accordance with the values obtained during the IET and the familiarization phase. CLT levels were 6 W for subject A, 10 W for subject B and 30 W for subject C. During the CLT subjects A and B could not follow the target work rate even with full effort. Therefore, work rate was reduced to 5 W for Subject B and he then could follow the target for 285 s. Subject A could not follow the reduced work rate and the test was terminated after 160 s. In contrast subject C was able to follow the target work rate with high accuracy. The setup and the testing were done within 2 h for each subject (Table 2). Limited efficacy (ii): In the IET subjects A and B reached their peak performance 247 s and 400 s after the start of the ramp, respectively, at which point they could not follow the target work rate for more than 20 s, and the IET was terminated. Subject C was able to follow the target work rate until the end of the test (Figure 3). The final level of perceived exertion was reported as 3 for subject A, 5 for subject B and 7 for subject C. The GET was estimated as 547 ml/min for subject A, 700 ml/min for subject B and 1564 ml/min for subject C (Figure 4). In the CLT the oxygen uptake kinetics in all three subjects followed an approximately exponential rise at the onset of

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Figure 3. IET responses for all three subjects. The first row shows the VO2 and the VCO2 kinetics. Each point represents a 15-breath average. The second row shows the heart rate and the third row shows the mechanical work rate. The dotted line (Pmech ) and the solid line (Pmech) were presented on the feedback screen in real-time.

Figure 4. Determination of gas exchange threshold (GET) of subject C in the incremental exercise test. The two dashed lines are two linear fits to determine the anaerobic threshold according to the v-slope method. The anaerobic threshold was found at 1564 ml/min VO2.

the load. In subject C a slow trend followed the initial rise (Figure 5). Subject C rated the level of perceived exertion as 6–7 at the beginning and as 8 at the end of the constant load phase. The mean HR in the CLT was higher than 90% of IET HRpeak in all _ 2 values relative to the previously estimated subjects. Mean VO _ 2 peak were 75% in subject A, 64% in Subject B and 90% in VO subject C. All key values for the IET and the CLT, except a valid oxygen uptake time constant for subject A, could be calculated (Table 3). (iii) Acceptability: the subjects’ feedback was mainly positive. All subjects agreed that the test was challenging and a good complement to the general rehabilitation programme. Subject B

Figure 5. The VO2 uptake kinetics at the onset of the active phase of the CLT of subject C. The points represent the unfiltered VO2 values for each breath in the first 200 s of the active phase. The solid line is a best fit function (y ¼ 485.3 + (1  e(t/ )) * 968.7; R2 ¼ 0.69, p ¼ 0.95) of these values. The dashed line marks the time constant of the oxygen uptake response (VO 2 ). Table 3. Summary of primary outcomes for limited efficacy testing _ 2 – oxygen uptake; HR – heart (feasibility assessment criterion (i)). VO rate; CLTss – steady-state value during the constant load test; IETpeak; peak value during the incremental exercise test; D – delta (increment) above passive. Subject _ 2 (ml/min) VO

HR (beats/min)

Rest CLTss (D) IETpeak (D) Rest CLTss (D) IETpeak (D)

A

B

C

302 470 (139) 606 (266) 91 124 (13) 137 (22)

352 517 (141) 819 (424) 62 85 (14) 94 (32)

488 1688 (1052) 1866 (1187) 88 142 (32) 153 (44)

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DOI: 10.3109/17483107.2014.908246

reported back pain and an uncomfortable feeling during the CLT and the test was terminated.

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Discussion The aim of this work was to assess the feasibility of a novel workrate-guided RTT intervention for cardiopulmonary training and assessment in subjects with iSCI with a view to deciding whether further efficacy testing of the work-rate guided RTT approach is warranted. The study used a small but representative sample of three patients with iSCI at distinct stages of primary rehabilitation. Given the consistency of the results, this small sample size is deemed appropriate in regard to the feasibility nature of the questions posed in the study design. The three subjects are representative because they were selected from the three distinct stages of a standardised primary rehabilitation programme: bodyweight-supported gait training on a treadmill (Lokomat), gait training using parallel bars, and overground gait training. Feasibility assessment focused on implementation, limited efficacy testing and acceptability: (i) Implementation. All three subjects were able to apply force on the thigh cuffs in order to increase their work rate and they were all able to vary their work rate to follow the target work rate displayed on the screen. The cardiopulmonary test protocol comprised a familiarisation phase, an IET and a CLT, all within a single 2-h test session. It is not ideal to carry out two cardiopulmonary tests within a single session, or even on the same day, because an appropriate recovery period is required; it is likely that the magnitude and duration of responses observed during the CLT will have been adversely affected by the preceding IET. Nevertheless, the CLT responses were substantial and sufficient to contribute to evaluation of limited efficacy testing of the RTT approach in line with the first aspect of feasibility assessment. Thus, it was deemed neither appropriate nor necessary to require subjects to attend for measurements on one additional day. (ii) Limited efficacy testing. The cardiopulmonary responses observed during the active part of CLTs and IETs were substantial. The findings of this study thus support the observations of previous studies: passive movement on a RTT activated the cardiovascular system to some extent [13]; for roboticsassisted treadmill exercise (Lokomat), active participation was found to evoke substantially higher cardiovascular responses, even in subjects with low performance levels [14,15]. The IET cardiopulmonary peak values for subjects A and B are rather low, consistent with their neurological status, but the intensity levels achieved in the CLT are still in the recommended range for effective aerobic training (50–80% HRmax) [2]. Considering the knowledge that the maximum HR in SCI subjects is lower compared to healthy subjects and peak values are strongly related to the lesion level [26,27], it can be said that the intensity during the CLT was high enough for aerobic training [28]. The calculation of the GET was carried out using the v-slope method according to Beaver et al. [29]. Although there were clearly detectable changes in the slope, the GET results from subjects A and B in particular have to be interpreted with caution, since this kind of test has to be validated first and anaerobic threshold calculations are known to have some limitations [30]. Although less is known about the validity of the CR-10 or CR-20 Borg scale in iSCI subjects, we let the subjects rate their perceived exertion at the beginning and the end of both tests according the CR-10 Borg scale [25]. By comparing these values with the physiological data, the perceived intensity of the tests could be better classified. The Borg values of subjects B and C seem to be well correlated with the HR values and similar

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to values reported in other studies [31,32]. The Borg values of subject A seem to be too low compared to the HR values. Al-Rahamneh et al. [32] observed that untrained SCI subjects show weaker rating results, which might be explained by the difficulty to distinguish between coordinative and physical efforts. However, RPE may be a good way to estimate subjects’ perceived exertion level. (iii) Acceptability. The exercise was generally tolerated well by all subjects. Subject A, the weakest subject at the earliest stage of rehabilitation, reported that the exercise was mainly a coordinative challenge rather than a physical endurance task. Due to the lack of somatosensory feedback, he found difficulty in synchronising leg-muscle activation with the movement of the leg drives and had to rely on observing the position of his legs. This situation might be alleviated by providing additional information regarding leg position on the visual feedback screen. The CLT for subject B was terminated prematurely as a result of discomfort in the back. That the performance level was too high can be excluded, as similar symptoms appeared in regular passive Lokomat sessions with this subject. As noted, the CLT followed a familiarisation phase and an IET in a single session and the overall duration was probably too long for this subject.

Conclusion The novel work-rate guided RTT intervention is deemed feasible for cardiopulmonary training and assessment in patients with iSCI: substantial cardiopulmonary responses were observed and the approach was found to be tolerable and implementable. The results were consistent for all three categories of subject studied. Based on this evidence, the approach is recommended for further efficacy testing: future work-rate guided RTT studies should focus on the one hand on iSCI subjects at an earlier stage of the rehabilitation process, since this device is able to stabilize subjects adequately, and on the other hand on comparative studies to obtain reference peak and endurance data.

Declaration of interest The authors declare no conflicts of interests. The authors alone are responsible for the content and writing of this article.

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Work-rate-guided exercise testing in patients with incomplete spinal cord injury using a robotics-assisted tilt-table.

Robotics-assisted tilt-table (RTT) technology allows neurological rehabilitation therapy to be started early thus alleviating some secondary complicat...
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