The official journal of the Korean Society for Neurorehabilitation (KSNR), and Asia-Oceanian Soceity for Neurorehabilitation (AOSNR)
pISSN 1976-8753 eISSN 2383-9910
Open Access, Peer-reviewed
Indexed in PubMed, PubMed Central, DOAJ and Korea Citation Index (KCI)
    Brain Neurorehabil. 2023 Mar;16(1):e9. English.
    Published online Mar 31, 2023.
    https://doi.org/10.12786/bn.2023.16.e9
    Copyright © 2023. Korean Society for Neurorehabilitation
    Original Article

    Cardiopulmonary Response to Robot-Assisted Tilt Table With Regard to Its Components

    Myeong Sun Kim,1 Ha Yeon Kim,2 Gyulee Park,1 Tae-Lim Kim,3 and Joon-Ho Shin3
      • 1Department of Rehabilitative and Assistice Techonology, Rehabilitation Research Institute, National Rehabilitation Center, Ministry of Health and Welfare, Seoul, Korea.
      • 2Department of Healthcare and Public Health Research, Rehabilitation Research Institute, National Rehabilitation Center, Ministry of Health and Welfare, Seoul, Korea.
      • 3Department of Rehabilitation Medicine, National Rehabilitation Center, Ministry of Health and Welfare, Seoul, Korea.
    • Correspondence to Joon-Ho Shin. Department of Rehabilitation Medicine, National Rehabilitation Center, Ministry of Health and Welfare, 58 Samgaksan-ro, Gangbuk-gu, Seoul 01022, Korea. Email: asfreelyas@gmail.com
    Received February 15, 2023; Revised March 24, 2023; Accepted March 24, 2023.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Cardiopulmonary function is exceptionally critical during the early stages of rehabilitation after neurological disorders such as stroke, spinal cord injury and Parkinson’s disease. This study aimed to demonstrate how robot-assisted and tilt table exercises affect cardiopulmonary function. In this study, ten healthy young adults performed six combinations of conditions according to robot-assisted mode (on/off), angle of tilt table (20°/60°), and functional electrical stimulation (FES) mode (on/off). Four conditions had FES mode off with combinations of robot-assisted mode (on/off) and tilt angle (20°/60°) and two conditions had robot-assisted mode and FES on with tilt angle (20°/60°). Cardiopulmonary effects (oxygen uptake [VO2], peak oxygen uptake [VO2peak], metabolic energy cost [MET], rate pressure product [RPP], heart rate [HR], maximum heart rate [%HRmax], and minute ventilation [VE]) were compared in each condition. As a result, in the angle and FES mode effect, VO2, VO2peak, MET, RPP, HR, and %HRmax, unlike that for VE, showed major effects in angle. In addition, in the robot-assisted mode and angle effect, when the FES was switched off, VO2, METs, and VE values showed major effects in the robot-assisted mode, whereas all other values showed major effects in angle. Compared to earlier reported findings, we can expect that robot-assisted tilt table training can lead to changes in the cardiopulmonary function.

    Graphical Abstract

    Highlights

    • · Cardiopulmonary function often deteriorates post intensive care admittance.

    • · This deterioration calls for immediate effective rehabilitation.

    • · Rehabilitation allows for proper cardiopulmonary function preservation.

    • · Robot-assisted tilt table (RATT) is suggested as rehabilitation.

    • · Cardiopulmonary function has been found to majorly benefit from RATT.

    Keywords
    Stroke; Robotics; Oxygen Consumption; Rehabilitation

    INTRODUCTION

    Cardiopulmonary function deteriorates in various conditions, especially following acute care of the condition. For instance, 1 month after the onset of stroke, maximum oxygen uptake (VO2max) decreases to 10–17 mL/kg/min and does not exceed 20 mL/kg/min for 6 months [1, 2]. Similarly, patients who complete intensive care suffer from post-intensive care syndrome, including weakness of the lower limbs and respiratory muscles as well as cardiopulmonary function deterioration. Spinal cord injury (SCI) and Parkinson’s disease (PD) also manifest decreased cardiopulmonary capacity, affecting quality of life and mortality [2, 3, 4, 5, 6]. Cardiopulmonary dysfunction is a major hurdle to participation in rehabilitation programs, and early rehabilitation is linked to good functional outcomes, including body function, muscle strength, and quality of life [7, 8, 9, 10]. Therefore, early intervention and the maintenance of cardiopulmonary function are major rehabilitation concerns.

    Various approaches have been adopted to improve the cardiopulmonary function [11]. Exercise, including resistance training, high-intensity interval training, continuous aerobic training, and inspiratory muscle training, has been recommended, and leg cycles or arm ergometers, treadmills, bicycles, and functional electrical stimulation (FES) have been widely utilized [9, 12, 13]. With advances in technology, robot-assisted exercises have been widely used, providing new access to rehabilitation programs for participants with cardiopulmonary dysfunction. The robot-assisted tilt table (RATT), which consists of a conventional tilt table and robot-assisted stepper, has demonstrated effectiveness in various conditions, including patients with spinal cord injury, stroke, and Parkinson’s disease [14, 15, 16, 17, 18, 19]. RATT usually targets patients with FES who find it difficult to access conventional treatments. It has been reported that RATT is effective in increasing cardiopulmonary response [20, 21, 22, 23]. Tilting table activates blood pressure response, and FES and passive robotic assisted movement activate skeletal muscle pumping, enhancing blood flow.

    Its application is crucial because RATT has adjustable elements, such as robot-assisted mode, tilting angle, and FES. Therefore, it is necessary to explore the changes in cardiopulmonary function according to each combination of these elements; these results will help determine the mode that can effectively promote cardiopulmonary function. This study aimed to explore the cardiopulmonary response according to the combination of each element of the RATT in a healthy young population.

    MATERIALS AND METHODS

    Participants

    A total of ten healthy young adults (seven males and three females; 25.2 ± 0.6 years old; weight, 71.5 ± 10.5 kg; height, 175.7 ± 7.7 cm) participated in this study. Participants on medication or those with cardiopulmonary diseases and/or musculoskeletal problems were excluded. All participants were recruited from the National Rehabilitation Center in the Republic of Korea, and the experiment was performed at the same center between June 2018 and August 2018. This study was approved by the institutional review board of the rehabilitation hospital, and all participants provided written informed consent prior to enrolment.

    Study design

    This study followed a cross-sectional design, and all participants conducted six conditions in random order in one day. Each session comprised different combinations depending on the angle (20° or 60°), robot-assisted mode (robot, on/off), and FES mode (FES, on/off) (Table 1). The study conditions in which the FES mode was on without robotic assistance were not set according to the study purpose. Each condition lasted for 5 minutes, and 5 minutes of rest time was provided between each condition. Each condition was randomly presented to the participants (Fig. 1). Appropriate measurements were taken for each condition as well as for resting time. Participants were instructed to relax and not exert any muscle contractions during the experiment. In addition, they were requested to restrict caffeine, alcohol, and exercise for 24 hours prior to the study.

    Table 1
    Experimental conditions, according to robot-assisted mode, degree of angle, and FES-mode

    Fig. 1
    An example of experiment protocol. Each condition was randomly presented to the participants.
    VO2, oxygen uptake; VO2peak, peak of oxygen uptake; MET, metabolic energy cost; RPP, rate pressure product; HR, heart rate; %HRmax, maximum of heart rate; VE, minute ventilation.

    Equipment

    Robot-assisted steppers with tilt tables (Erigo Pro, Hocoma AG, Switzerland) have armrests, footrests, and adjustable belts for stabilizing the trunk and both legs (Fig. 2). The angle of the equipment is adjustable (0° to 90°), and the guidance force and cadence can be adjusted according to the patient’s power and speed. The guidance force was set to 100% to ensure an absolute passive movement and speed at a cadence of 28 steps/min.

    Fig. 2
    Robot-assisted stepper with a tilt table (Erigo Pro).

    The FES system was attached to the biceps femoris, vastus medialis, tibialis anterior, and gastrocnemius muscles. Like our study conditions, in the absence of electrical flow, it was activated according to the movement of the stepper. The intensity of the FES was set at 10–14mA without subject discomfort.

    Outcome measurements

    Gas analysis was performed to obtain diverse parameters related to the cardiopulmonary response. It was performed throughout the duration of the conditions, and the outcomes of the middle 3 min of each condition were used as average values. Blood pressure (BP) and heart rate (HR) were measured at the 3 min of each session of every condition, totaling six times. Gas exchange was measured using a breath-by-breath gas analyzer system (Quark K4B2 system; COSMED, Rome, Italy), and BP and HR were measured using a sphygmomanometer (HEM-7310, OMRON, Shanghai, China). Gas analyzer data were measured during the conditions, and the average outcome during the middle of 3 min from each condition was used. Gas exchange analysis provided the oxygen uptake (VO2), metabolic energy cost (mL/kg/min; MET), and ventilatory response (minute ventilation; VE). Peak oxygen uptake (VO2peak) was obtained from the highest value during the 3 minutes.

    The rate pressure product (RPP) was calculated using the equation (systolic BP × HR)/100 and used instead of myocardial oxygen consumption (MVO2) to avoid invasive measurement and the difficulty of continuous wearing of masks for gas analysis. The expected maximum HR (HRmax) was calculated using the equation (220 - age) and used to obtain the percentage of Hrmax using an equation measuring HR/Hrmax.

    Statistical analysis

    All data were analyzed using two approaches because this study mainly focused on robotic manipulation. Most of the variables satisfied normality, thus two-way repeated measures analyses of variance (RM ANOVA) were utilized to compare the variables according to the angles (20° or 60°) and mode of robotics (on/off) with the FES mode off. We then used RM ANOVA to compare the variables according to the angles (20° or 60°) and the FES mode (on/off) with the robot-assisted mode on. All statistical analyses were performed using SPSS version 20.0 (IBM Corporation, Armonk, NY, USA), and statistical significance was set at p < 0.05.

    RESULTS

    Effects of robot, angle, and robot × angle interactions while FES is switched off

    We compared the effects of the robot or angle on the outcome measurements when the FES was off. For VO2, VE, and METs, a marked main effect of the robot-assisted mode was observed, whereas no main effect of the angle was noted. Moreover, no effect of the robot × angle interaction was found on these variables. For VO2peak, no main effects of the robot, angle, or robot × angle interaction were noted. As for RPP, HR, and %HRmax, main effects of the angle, whereas no main effects of the robot, were observed. Furthermore, no robot × angle interactions for these variables were found (Table 2). The higher the angle, the higher the value of the cardiopulmonary variables were observed when the robot mode was on. VO2 values were 3.88 ± 0.97 (condition 1), 3.90 ± 0.89 (condition 2), 4.16 ± 1.00 (condition 3), and 4.37 ± 0.87 (condition 4). MET values were 1.11 ± 0.27 (condition 1), 1.11 ± 0.25 (condition 2), 1.19 ± 0.28 (condition 3), and 1.25 ± 0.25 (condition 4). RPPs values were 89.08 ± 17.03 (condition 1), 101.68 ± 20.1 (condition 2), 81.1 ± 20.98 (condition 3), and 106.15 ± 20.37 (condition 4).

    Table 2
    Two-way repeated measures analyses of variance of angle and robot-assisted mode

    Effects of angle, FES, and angle × FES interactions while robot is switched on

    We then compared the effects of the angle or FES on the outcome variables when the robot was on. There were main effects of the angle on all outcomes, whereas no main effects of the FES or angle × FES interactions were observed (Table 3). When the robot was on, the variables tended to be higher with a higher angle, regardless of whether FES was on or off. VO2 values were 4.16 ± 1.00 (condition 3), 4.37 ± 0.87 (condition 4), 3.88 ± 0.97 (condition 5), and 3.90 ± 0.89 (condition 6). MET values were 1.19 ± 0.28 (condition 3), 1.25 ± 0.25 (condition 4), 1.19 ± 0.28 (condition 5), and 1.3 ± 0.27 (condition 6). RPP values were 81.1 ± 20.98 (condition 3), 101.15 ± 20.37 (condition 4), 86.87 ± 15.82 (condition 5), and 100.56 ± 18 (condition 6).

    Table 3
    Two-way repeated measures analyses of variance of angle and functional electrical stimulation mode

    DISCUSSION

    In this study, we demonstrated that the cardiopulmonary response was considerably higher when the robot-assisted mode was on and that the cardiopulmonary response was dependent on the angle. In the robot-assisted mode conditions, the effects of the angle were notable on cardiopulmonary responses, whereas the effects of FES on cardiopulmonary function were not significant.

    A higher cardiopulmonary response was obtained when the robot-assisted mode was on, although we set 100% of the guidance force. This indicates that even passive movements result in a higher cardiopulmonary response. However, the robot-assisted mode did not produce a cardiopulmonary response, as measured using the RPP, HR, and %maxHR. This discrepancy might be because the robot-assisted mode was passive, and the participants did not make any exertion; hence, the cardiopulmonary response was not sufficient to make a significant change. Previous studies demonstrated that active robotic training led to a greater cardiopulmonary response than passive robotic training [16, 17]. The RATT used in the present study (Erigo Pro) is capable of an active-assistive mode in which the movement of the robot occurs by detecting muscle movements, and the guidance force can be adjusted. Therefore, it would be better to apply robot-assisted mode to patients with reduced cardiorespiratory function, and if possible, it would be better to provide an active robotic training.

    In addition, the tilting angle extensively affected the cardiopulmonary response when the robot-assisted mode was switched on. This response is derived from the effect of gravity and the action of the sympathetic autonomic nervous system. The 45° upright posture bicycle showed a higher cardiopulmonary response including VO2peak, HRpeak, and VE than the 0° supine posture bicycle [18]. In addition, the cardiorespiratory response increases with increasing tilt angles [19, 24, 25]. Therefore, increasing the tilting angle for verticalization may be recommended according to the patient’s cardiopulmonary function.

    Although the effect of FES on cardiopulmonary function was not significant in this study, previous studies have reported contradictory results. A previous study comparing whether FES was applied to a leg-cycling wheelchair demonstrated no significant differences for all variables, indicating no significant effects of FES on energy cost [18, 26]. In contrast, the application of passive activity and FES has demonstrated positive effects on cardiorespiratory responses and oxygen utilization in stroke, spinal cord injury and cardiovascular disease patients [19, 26, 27, 28, 29, 30]. Despite these inconsistent cardiopulmonary response results, FES combined with robotic training might be meaningful for other functions, such as muscle strength, postural control, and stepping, as well as cardiovascular functions [31, 32, 33].

    The value related to cardiopulmonary response was low, in which the maximal mean VO2 was 4.37 ± 0.87 mL/kg/min and percentage of HRmax was 39.54 ± 5.36%. The American College of Sports Medicine guidelines recommend an appropriate aerobic training intensity of 60%–80% of VO2max and 50%–85% of HRmax. For cardiopulmonary function improvement, moderate to maximal intensity is required, which can reach 40%–59% VO2 reserve (VO2R) [34]. Similarly, all the values obtained in this study were far below the required intensity. Altogether, it seems that the RATT administered to the subjects was not sufficient to affect cardiopulmonary function. In a previous study, RATT use in 11 healthy adults found that the 70° tilting and passive movement at a frequency of 80 steps/min induced 1.3 times higher VO2 of passive movement than resting VO2, however, not sufficient to produce a meaningful cardiopulmonary response [35].These results might be because this experiment was performed in a young, healthy population; thus, the cardiopulmonary response might be more meaningful for participants with severely deteriorated cardiopulmonary functions. RATT use in six SCI patients demonstrated that active participation of RATT showed a considerable increase in VO2, VE, and HRs [17]. Moreover, the benefits of RATT as a passive range of motion exercise, the prevention of orthostatic hypotension, and the maintenance of muscle mass are especially valuable in the early stages of rehabilitation.

    Our study has some limitations. First, the present results cannot be directly applied to patients with impaired cardiopulmonary function because this study was performed with a small number of healthy young participants. Second, we did not measure other outcomes of motor function, such as range of motion, muscle strength, or mobility. In addition, we explored only immediate physiological changes rather than long-term changes. Third, we did not include active-assisted or active-robot modes; thus, the effects of the robot-assisted mode may have been minimized. Finally, 5 min resting period was set to wash out the effect of the previous exercise. However, this may not have provided sufficient rest and still affected the next exercise. Nevertheless, the exercise intensity was not high enough to raise the RER above 1.1, and all conditions were randomized. Therefore, the aftereffects of previous exercise might have been negligible. More studies are warranted to explore these possible benefits for patients with disabilities and very limited functions for early-stage rehabilitation and to prevent deconditioning.

    Application of the appropriate RATT mode is important for maintaining cardiopulmonary function. This study showed the RATT use induced higher cardiopulmonary response in having robot-assisted mode with a high angle. Based on the findings of this study, robot-assisted mode and tilting angle are major factors in the cardiopulmonary response. This implies that the cardiopulmonary effects of robot-assisted mode and angle should be considered when designing intervention programs.

    Notes

    Funding:This study was supported by grants (NRCTR-IN18001 and NRCTR-IN19001) from the Translational Research Program for Rehabilitation Robots, National Rehabilitation Center, Ministry of Health and Welfare, Korea.

    Conflict of Interest:The authors have no potential conflicts of interest to disclose.

    Data Availability Statement:The datasets used in this study are available from the corresponding author upon reasonable request.

    Author Contributions:

    • Conceptualization: Shin JH.

    • Data curation: Kim HY, Park G.

    • Formal analysis: Shin JH.

    • Investigation: Kim MS, Kim HY, Park G, Kim TL, Shin JH.

    • Writing - original draft: Kim MS.

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    MeSH Terms
    Electric Stimulation
    Exercise
    Heart Rate
    Humans
    Nervous System Diseases
    Oxygen
    Oxygen Consumption
    Rehabilitation
    Robotics
    Spinal Cord Injuries
    Stroke
    Tables*
    Ventilation
    Young Adult
    Metrics
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