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Article

Cardiorespiratory Responses to 10 Weeks of Exoskeleton-Assisted Overground Walking Training in Chronic Nonambulatory Patients with Spinal Cord Injury

1
Department of Rehabilitation Medicine, Hanyang University Guri Hospital, 153 Gyeongchun-ro, Guri-si 11923, Korea
2
Department of Rehabilitation Medicine, Hanyang University College of Medicine, 222-1 Wangsimni-ro, Seoul 04763, Korea
3
Robotics Lab, R&D Division of Hyundai Motor Company, 37 Cheoldobangmulgwan-ro, Uiwang-si 16082, Korea
*
Author to whom correspondence should be addressed.
Submission received: 14 June 2021 / Revised: 15 July 2021 / Accepted: 21 July 2021 / Published: 24 July 2021
(This article belongs to the Special Issue Rehabilitation Robots and Sensors)

Abstract

:
Exercise intensity of exoskeleton-assisted walking in patients with spinal cord injury (SCI) has been reported as moderate. However, the cardiorespiratory responses to long-term exoskeleton-assisted walking have not been sufficiently investigated. We investigated the cardiorespiratory responses to 10 weeks of exoskeleton-assisted walking training in patients with SCI. Chronic nonambulatory patients with SCI were recruited from an outpatient clinic. Walking training with an exoskeleton was conducted three times per week for 10 weeks. Oxygen consumption and heart rate (HR) were measured during a 6-min walking test at pre-, mid-, and post-training. Exercise intensity was determined according to the metabolic equivalent of tasks (METs) for SCI and HR relative to the HR reserve (%HRR). Walking efficiency was calculated as oxygen consumption divided by walking speed. The exercise intensity according to the METs (both peak and average) corresponded to moderate physical activity and did not change after training. The %HRR demonstrated a moderate (peak %HRR) and light (average %HRR) exercise intensity level, and the average %HRR significantly decreased at post-training compared with mid-training (31.6 ± 8.9% to 24.3 ± 7.3%, p = 0.013). Walking efficiency progressively improved after training. Walking with an exoskeleton for 10 weeks may affect the cardiorespiratory system in chronic patients with SCI.

1. Introduction

Spinal cord injury (SCI) occurs in 0.93 million persons per year worldwide, and the age-standardized incidence rate is 13 per 100,000 people, causing a significant global injury burden [1]. Patients with SCI suffer from various health conditions, including pain, pressure ulcers, depression, bladder and bowel dysfunctions, impaired proprioception, and motor weakness [2,3]. Patients with SCI often have difficulty in walking due to motor weakness or impaired proprioception, which can lead to significant reductions in physical activities and a sedentary lifestyle [3,4]. Consequently, individuals with SCI have an increased risk of cardiovascular diseases [2,4]. Moreover, cardiovascular diseases have become a major cause of mortality in individuals with chronic SCI [5]. Therefore, lifestyle interventions have become an important issue in reducing cardiovascular mortality in patients with SCI [6].
Physical activity is an approved lifestyle intervention for cardiovascular fitness in patients with chronic SCI [4,6,7]. Exercise guidelines recommend at least 30 min of moderate to vigorous aerobic exercise three times a week to maintain cardiometabolic health [7,8]. Arm crank or wheelchair sports, such as wheelchair basketball or tennis, are common aerobic exercises for patients with chronic SCI who are wheelchair-dependent [4]. However, many individuals with SCI do not sufficiently participate in these exercises [9]. Furthermore, all these exercises are performed in a sitting position.
Robotic exoskeletons have been developed for individuals with difficulty in ambulation as an assistive gait training device and for personal use in daily activities [10,11]. Robotic exoskeletons provide external body weight support and lower extremity propulsion, which help non-ambulatory patients to walk. Furthermore, there has been growing interest in the use of robotic exoskeletons as an exercise modality. Walking training with a robotic exoskeleton is performed in a standing position, which has been reported to have many health and psychological benefits such as improved bowel function, blood circulation, quality of life, and better self-image [12]. Additionally, it has been reported that walking with an exoskeleton can elicit activation of trunk muscles below the level of injury, implying that more muscles may be recruited during exoskeleton-assisted walking than activities performed in sitting position [13]. Previous studies have demonstrated that, according to cardiorespiratory responses, the exercise intensity of walking with a robotic exoskeleton is moderate in patients with SCI despite different training sessions performed before measurements [14,15,16,17,18,19]. Although long-term physical activity with a moderate intensity level is known to induce positive cardiorespiratory responses, most studies have not reported changes in cardiorespiratory responses after exoskeleton-assisted walking training with improved proficiency in exoskeleton use. Only a few case studies have reported the changes in cardiorespiratory responses to six weeks of exoskeleton-assisted walking training [18,20]. However, these case studies reported inconsistent results and could not provide definite conclusions on the cardiorespiratory changes that occur in response to long-term exoskeleton use.
To date, the knowledge of the changes in cardiorespiratory responses to robotic exoskeleton-assisted overground walking training is limited. Thus, the purpose of this study was to investigate the exercise intensity of overground walking training with a robotic exoskeleton and to assess the changes in cardiorespiratory responses to robotic exoskeleton-assisted overground walking training in chronic nonambulatory patients with SCI.

2. Materials and Methods

2.1. Trial Design and Participants

This was a single-center, prospective, single-group observational study. Nonambulatory participants with SCI were recruited from an outpatient clinic in the rehabilitation department of a tertiary hospital. As this study is part of an early feasibility study for a newly developed exoskeleton, the sample size was determined to be 10 participants [21,22]. Functional improvement after exoskeleton-assisted walking has recently been published [21]. In this study, we focused on changes in cardiorespiratory responses after exoskeleton-assisted walking training. The inclusion criteria were (1) neurologically stable SCI without a change of motor or sensory level at least two months since injury, (2) age > 18 years, (3) body weight < 110 kg, (4) height between 1.6 and 1.8 m, (5) sufficient postural stability to perform a level transfer, and (6) sufficient upper-extremity strength to use a walker or crutch. The exclusion criteria were (1) spinal instability, (2) severe joint contracture in the lower extremities, (3) unhealed fracture in the lower extremities, (4) skin injuries in areas of contact with the device, (5) unresolved deep vein thrombosis, (6) uncontrolled hypertension or hypotension, (7) severe osteoporosis or osteoporotic fracture that could interfere with gait training, (8) spasticity of the lower extremities exceeding 3 out of 4 on the modified Ashworth scale, (9) functional limitation in the upper extremities due to weakness or contracture, (10) psychological or cognitive problems that may limit the ability to understand the investigator’s instructions, and (11) any other issue that may interfere with the trial.

2.2. Exoskeleton and Training

The Hyundai Medical Exoskeleton (H-MEX; Hyundai Motor Company, Uiwang-si, Korea) was used in this study. A detailed description of the H-MEX has been previously reported [21,23]. H-MEX weighs approximately 19 kg, generates walking propulsion via actuators for flexion/extension in the hip and knee joints, and provides locomotive stability by way of hip abduction during hip flexion and hip adduction during hip extension via abduction/adduction actuators for the pelvic joints. Locomotive stability was also achieved by using a ground reaction force sensor-based permission operation. The exoskeleton was adjusted to each participant’s length of the lower extremities (thigh and shank) and position of the joints (hip, knee, and ankle) before training. Walking was initiated and stopped using the controller in the crutch hand grip. The bipedal gait was initiated by pressing the button on the left crutch with unilateral forward movement and stopped by pressing another button on the left crutch.
Before the walking training, the participants were provided with a detailed explanation of how to handle the exoskeleton and underwent a pre-training session to adapt to the use of the exoskeleton. The training program was performed for a total of 30 sessions, with a 60-min duration, three times a week for 10 weeks. The training program consisted of sit-to-stand, walking, and stand-to-sit movements. The participants walked along a flat 20-m corridor under the researchers’ close supervision. At the end of the corridor, the turn was made by changing direction little by little with the assistance of the researcher. The participants were allowed to rest in a sitting position during the walking training session, as needed. During the training, an overhead harness system (LG-1000; Neotech Inc., Gimpo-si, Korea) was loosely connected to the exoskeleton without weight support to prevent falls. As the training progressed, the walking distance and walking time without rest gradually increased, and the researchers’ level of assistance gradually decreased.

2.3. Measurements

2.3.1. Six-Minute Walking Test (6MWT)

Walking ability was assessed using the 6MWT at the pre-, mid- (at week 5, after 15 training sessions), and post-training time (after 30 training sessions) points during the exoskeleton training [24]. The initial 6MWT distance was measured after one to three acclimating sessions before the walking training began to allow the participants to become accustomed to the exoskeleton. Before the 6MWT, the participants were asked to rest in a sitting position for more than 5 min. The participants ambulated along a 20 m straight walkway, which was used as a training path. The 6MWT began with the first step. The participants made a turn at the end of the corridor. Resting was allowed during the 6MWT. The number and duration of rests were not recorded. The time taken to turn around at the end of the corridor and the resting time were both included in the 6MWT. If the participants wanted to discontinue walking, the test was terminated and the distance at that time was recorded. Walking speed was determined by dividing the total walking distance by six minutes (m/min).

2.3.2. Cardiorespiratory Measurements

Cardiorespiratory assessments were performed at pre-, mid-, and post-training time with the 6MWT. Cardiorespiratory measurements were obtained using the Metamax 3B portable gas analysis system (Cortex Medical, Leipzig, Germany) (Figure 1), which has been shown to be reliable and valid [25]. Prior to testing, calibration was performed according to the manufacturer’s guidelines. The respiratory measurements and heart rates for the breath-by-breath data were taken every 3 s. Cardiorespiratory measurements included volume of oxygen consumption (VO2, mL/kg/min) and heart rate (HR, beats/min). VO2 was determined using standard metabolic algorithms, and HR was measured using a polar belt. The data were analyzed using Metasoft 3 software. Before the 6MWT, VO2 during rest (VO2rest) and HR during rest (HRrest) were measured while wearing the exoskeleton during a 1-min of resting period. The highest VO2 (VO2peak) and HR (HRpeak) values were measured during the 6MWT. The average VO2 (VO2avg) and HR (HRavg) values for the entire 6MWT were calculated. Cardiorespiratory measurements were not assessed separately for each movement of walking, turning or rest during the 6MWT.

2.4. Data Analysis

2.4.1. Exercise Intensity and Walking Efficiency

First, exercise intensity was evaluated using the metabolic equivalent of tasks (METs) and the Karvonen method [26]. We set 1 MET as 2.7 mL/kg/min for participants with SCI [27] and classified the exercise intensity based on the METs into low (<3 METs), moderate (3–6 METs), and vigorous (>6 METs) levels [27,28]. The highest METs (METpeak) and average METs (METavg) during the 6MWT were calculated. Second, exercise intensity was also determined using the Karvonen method, with HR relative to the HR reserve (%HRR) [26,28]. The %HRR was calculated as the difference between HRrest and the age-predicted maximal HR, as shown in Equation (1). Exercise intensity according to the %HRR was categorized into light (30–39%), moderate (40–59%), and vigorous (60–89%) levels [8,26,28]. Third, walking efficiency was estimated using the oxygen cost of walking (O2walking), calculated as VO2 divided by walking speed (m/min) [17]. O2walking refers to the amount of oxygen consumed per 1 kg of body weight to walk a 1-m distance.
% HRR   = current   HR     HR r e s t age   predicted   maximal   HR     HR r e s t × 100 = current   HR     HR r e s t 220   age   HR r e s t × 100 ,

2.4.2. Statistical Analysis

Friedman tests were conducted to compare the changes of outcome variables at pre-, mid-, and post-training. A p-value of <0.05 was considered statistically significant. After the Friedman test, post-hoc analysis was performed using a Wilcoxon signed rank test. The Bonferroni correction was used by adjusting the p-value for multiple comparisons (p < 0.05/3). Statistical analyses were performed using SPSS software version 24 (IBM/SPSS Inc., Armonk, NY, USA).

3. Results

3.1. Participants

Of the 19 participants who were screened, one was excluded due to insufficient postural stability, and another seven participants did not want to engage in the study for personal reasons such as scheduling conflicts or difficulty coming to the laboratory. Eleven participants were enrolled in this study, and one participant withdrew before the initial training session because of scheduling conflicts. A total of 10 participants completed the training sessions. The demographic characteristics and clinical information of the 10 participants are presented in Table 1. The participants included seven men and three women with age ranging from 35 to 63 years (mean ± standard deviation, 48.1 ± 8.7) and time since injury ranged from 1.1 to 15.6 years (mean ± standard deviation, 5.7 ± 4.8). All participants had intact upper-extremity motor function except for one participant with a C6 neurologic level of injury. However, this latter participant had sufficient upper-extremity strength (all upper-extremity muscle grade ≥ 4 out of 5) to conduct walking training with an exoskeleton.

3.2. Walking Distance

The results of the 6MWT and cardiorespiratory measurements are presented in Table 2. In the 6MWT, the participants walked a significantly further distance at mid-training (37.5 ± 10.5 m) than at pre-training (20.7 ± 5.5 m) (p = 0.005) and covered more distance at post-training (49.1 ± 15.2 m) than at pre- and mid-training (p = 0.05 and p = 0.014, respectively).

3.3. Cardiorespiratory Outcomes

VO2rest, VO2peak, and VO2avg were not significantly different after walking training. HRavg during the 6MWT at post-training (100.3 ± 10.7) decreased compared with that at pre-training (111.5 ± 17.2), at a borderline significance level (p = 0.028) and was significantly decreased compared with that at mid-training (110.0 ± 11.7) (p = 0.009).

3.4. Exercise Intensity and Walking Efficiency

The exercise intensity calculated according to cardiorespiratory outcomes and walking efficiency is provided in Figure 2. The categorization of exercise intensity is indicated by gray shading. The METpeak during the 6MWT at pre-, mid-, and post-training was 5.1 ± 1.3, 4.9 ± 0.7, and 4.9 ± 1.1, respectively (pre- vs. mid-, p = 0.959; pre- vs. post-, p = 0.799; mid- vs. post- p = 0.799), and the METavg was 3.3 ± 0.9 at pre-training, 3.5 ± 0.6 at mid-training, and 3.5 ± 0.7 at post-training (pre- vs. mid-, p = 0.285; pre- vs. post-, p = 0.445; mid- vs. post-, p = 0.646). There was no difference in the METpeak or METavg even after exercise.
The %HRRpeak changed from 43.4 ± 25.4% (pre-training) to 41.3 ± 11.1% (mid-training) to 39.6 ± 23.6 (post-training) (pre- vs. mid-, p = 0.959; pre- vs. post-, p = 0.575; mid- vs. post-, p = 0.074), and the %HRRavg changed from 32.2 ± 17.9% (pre-training) to 31.6 ± 8.9% (mid-training) to 24.3 ± 7.3% (post-training) (pre- vs. mid-, p = 0.799; pre- vs. post-, p = 0.114; mid- vs. post-, p = 0.013). O2walking significantly decreased from 2.7 ± 0.7 at pre-training to 1.6 ± 0.5 at mid-training to 1.2 ± 0.4 at post-training (pre- vs. mid-, p = 0.005; pre- vs. post-, p = 0.005; mid- vs. post-, p = 0.017).

4. Discussion

Our results demonstrated that the exercise intensity of walking with a robotic exoskeleton according to the METs (both peak and average) corresponded to a moderate level and did not change after 10 weeks of the walking training program, whereas the exercise intensity at pre-training according to the %HRRpeak and %HRRavg corresponded to a moderate and light level, respectively, and decreased after 10 weeks of the walking training program. Furthermore, walking efficiency gradually improved after walking training with a robotic exoskeleton.
The cardiorespiratory responses assessed using VO2 in this study were consistent with those reported in previous studies, which indicated that the metabolic demand of walking with an exoskeleton is equivalent to a moderate level of physical activity [14,15,17,19]. The number of training sessions varied among the studies; however, exercise intensity was similar. In previous studies, the exercise intensity of exoskeleton-assisted walking was measured after a minimum of five training sessions [14], after approximately 40 training sessions [15], or after 4–14 training sessions (median, 10 sessions) [17]. Furthermore, a meta-analysis study by Miller et al. [10] demonstrated that, using a MET value of 2.7 mL/kg/min for participants with SCI, the average exercise intensity during exoskeleton-assisted walking was 3.3 METs, which is comparable to the METavg in this study. However, the exercise intensity evaluated according to the HR was moderate (%HRRpeak) and less than moderate level (%HRRavg) in this study. Kozlowski et al. reported that exoskeleton-assisted walking corresponded to light to moderate exercise by estimating the METs using HR changes [16].
Several explanations could be proposed as to why the estimated exercise intensity of exoskeleton-assisted walking was different depending on the measurement methods. First, the reference value for estimating exercise intensity may be associated with these results. In this study, we used the reference value of the METs for patients with SCI (2.7 mL/kg/min), which is lower than that for healthy adults (3.5 mL/kg/min) [27]. Conversely, the %HRR was calculated using the age-predicted maximal HR (220-age), which was not adjusted for patients with SCI. In previous studies, the peak HR of patients with SCI was lower than the age-predicted maximal HR not only in patients with tetraplegia but also in patients with paraplegia [29,30]. Second, these results may be attributed to the innate characteristics of these measurement methods. The %HRR has been reported to have a tendency to underestimate exercise intensities, whereas the VO2 reserve tends to be overestimated in young healthy adults [31]. For these reasons, the exercise intensity calculated by %HRR may be underestimated compared to METs. Therefore, further research is needed to determine the reference value for %HRR in patients with SCI.
The results of the present study showed that VO2 did not changed, whereas HRavg and %HRRavg significantly decreased after 10 weeks of exoskeleton-assisted walking training. This is in agreement with the knowledge that regular aerobic exercise reduces the HR during submaximal workload due to decreased sympathetic drive and increased stroke volume, but does not change submaximal VO2 because of similar oxygen requirements for a fixed workload [32,33]. Although the activities of the trunk and upper extremity muscles were not evaluated in this study, it can be assumed that exoskeleton-assisted gait would be insufficient to induce muscle hypertrophy. Furthermore, despite the fact that exoskeleton-assisted walking training was not an overloading exercise, exoskeleton-assisted walking may be a tolerable aerobic exercise to induce cardiorespiratory responses considering the decrease in %HRRavg. In contrast, Kressler et al. reported no considerable changes in HR and VO2 during exoskeleton-assisted walking among three participants after six weeks of training [18]. These contradictory findings may have resulted from the duration of training, as other experimental designs including training methods, time, and frequency were similar between the previous study and this study. The duration of six weeks would be insufficient to make changes in cardiovascular activities, considering that no significant difference was observed in the HR or %HRR at week 5 in this study.
The energy cost for exoskeleton-assisted overground walking decreased after walking training. The progressive improvement in walking efficiency during the 10 weeks of training is a meaningful finding because faster exoskeleton-assisted walking may not require more metabolic demands as a result of walking proficiency. Further studies with larger sample sizes and training durations of >10 weeks are needed to identify the effects of walking training on walking efficiency and cardiorespiratory responses.
This study had some limitations. First, the study population was small and relatively heterogeneous, limiting the generalizability of the results. Second, cardiopulmonary exercise tests for evaluating maximal VO2 and HR were not conducted. Third, it was not possible to identify the effects of exoskeleton-assisted walking training for more than 10 weeks. Fourth, rest time during the 6MWT was not recorded, and cardiorespiratory responses during turn and rest were not assessed separately. Thus, the effects of rest and turning cannot be demonstrated. Finally, we did not assess how long the effects of exoskeleton-assisted walking for 10 weeks lasted after training.

5. Conclusions

Exoskeleton-assisted overground walking in patients with chronic SCI is generally compatible with a moderate level of physical activity. Regular walking training using an exoskeleton for 10 weeks progressively improves walking efficiency in chronic nonambulatory patients with SCI and may result in changes in cardiorespiratory responses.

Author Contributions

Conceptualization, M.J.K.; methodology, J.H.P.; software, D.J.H., S.I.P., J.Y. and H.L.; validation, J.H.P.; formal analysis, J.H.P.; investigation, H.S.K.; resources, D.J.H., S.I.P., J.Y. and H.L.; data curation, D.J.H., S.I.P., J.Y., H.L. and H.S.K.; writing—original draft preparation, J.H.P.; writing—review and editing, S.H.J. and M.J.K.; visualization, J.H.P.; supervision, S.H.J. and M.J.K.; project administration, J.H.P. and M.J.K.; funding acquisition, M.J.K. All authors have read and agreed to the published version of the manuscript.

Funding

This project was supported by the ‘‘Human Gait Assistance Project” in the R&D division of Hyundai Motor Company (no. 201600000002998).

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board of Hanyang Medical Center (IRB File No. 2017-01-050).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study. Written informed consent was obtained from the patient for publication of this paper.

Data Availability Statement

The data presented in the study are available upon request from the corresponding author. The data are not publicly available because of reasons concerning the privacy of the participants.

Acknowledgments

We thank the late Kyungmo Jung, who planned this study together with the authors.

Conflicts of Interest

As employees of the R&D division of Hyundai Motor Company, D.J. Hyun, S. Park, J. Yoon, and H. Lim have received salary support from Hyundai Motor Company. The other authors have no conflict of interest.

References

  1. GBD 2016 Neurology Collaborators. Global, regional, and national burden of traumatic brain injury and spinal cord injury, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2019, 18, 56–87. [Google Scholar] [CrossRef] [Green Version]
  2. Jensen, M.P.; Truitt, A.R.; Schomer, K.G.; Yorkston, K.M.; Baylor, C.; Molton, I.R. Frequency and age effects of secondary health conditions in individuals with spinal cord injury: A scoping review. Spinal Cord 2013, 51, 882–892. [Google Scholar] [CrossRef] [Green Version]
  3. Wirz, M.; van Hedel, H.J.A. Balance, gait, and falls in spinal cord injury. Handb. Clin. Neurol. 2018, 159, 367–384. [Google Scholar] [CrossRef] [PubMed]
  4. Jacobs, P.L.; Nash, M.S. Exercise recommendations for individuals with spinal cord injury. Sports Med. 2004, 34, 727–751. [Google Scholar] [CrossRef] [PubMed]
  5. Garshick, E.; Kelley, A.; Cohen, S.A.; Garrison, A.; Tun, C.G.; Gagnon, D.; Brown, R. A prospective assessment of mortality in chronic spinal cord injury. Spinal Cord 2005, 43, 408–416. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. DiPiro, N.D.; Cao, Y.; Krause, J.S. A prospective study of health behaviors and risk of all-cause and cause-specific mortality after spinal cord injury. Spinal Cord 2019, 57, 933–941. [Google Scholar] [CrossRef]
  7. Martin Ginis, K.A.; van der Scheer, J.W.; Latimer-Cheung, A.E.; Barrow, A.; Bourne, C.; Carruthers, P.; Bernardi, M.; Ditor, D.S.; Gaudet, S.; de Groot, S.; et al. Evidence-based scientific exercise guidelines for adults with spinal cord injury: An update and a new guideline. Spinal Cord 2018, 56, 308–321. [Google Scholar] [CrossRef] [Green Version]
  8. Riebe, D.; Ehrman, J.K.; Liguori, G.; Magal, M. ACMS’s Guidelines for Exercise Testing and Prescription, 10th ed.; Wolters Kluwer Health: Philadelphia, PA, USA, 2018. [Google Scholar]
  9. Ginis, K.A.M.; Latimer, A.E.; Arbour-Nicitopoulos, K.P.; Buchholz, A.C.; Bray, S.R.; Craven, B.C.; Hayes, K.C.; Hicks, A.L.; McColl, M.A.; Potter, P.J. Leisure time physical activity in a population-based sample of people with spinal cord injury part I: Demographic and injury-related correlates. Arch. Phys. Med. Rehabil. 2010, 91, 722–728. [Google Scholar] [CrossRef] [PubMed]
  10. Miller, L.E.; Zimmermann, A.K.; Herbert, W.G. Clinical effectiveness and safety of powered exoskeleton-assisted walking in patients with spinal cord injury: Systematic review with meta-analysis. Med. Devices 2016, 9, 455–466. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  11. Kandilakis, C.; Sasso-Lance, E. Exoskeletons for personal use after spinal cord injury. Arch. Phys. Med. Rehabil. 2019. [Google Scholar] [CrossRef]
  12. Rodriguez-Fernandez, A.; Lobo-Prat, J.; Font-Llagunes, J.M. Systematic review on wearable lower-limb exoskeletons for gait training in neuromuscular impairments. J. Neuroeng. Rehabil. 2021, 18, 22. [Google Scholar] [CrossRef] [PubMed]
  13. Alamro, R.A.; Chisholm, A.E.; Williams, A.M.M.; Carpenter, M.G.; Lam, T. Overground walking with a robotic exoskeleton elicits trunk muscle activity in people with high-thoracic motor-complete spinal cord injury. J. Neuroeng. Rehabil. 2018, 15, 109. [Google Scholar] [CrossRef]
  14. Evans, N.; Hartigan, C.; Kandilakis, C.; Pharo, E.; Clesson, I. Acute cardiorespiratory and metabolic responses during exoskeleton-assisted walking overground among persons with chronic spinal cord injury. Top. Spinal Cord Inj. Rehabil. 2015, 21, 122–132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Asselin, P.; Knezevic, S.; Kornfeld, S.; Cirnigliaro, C.; Agranova-Breyter, I.; Bauman, W.A.; Spungen, A.M. Heart rate and oxygen demand of powered exoskeleton-assisted walking in persons with paraplegia. J. Rehabil. Res. Dev. 2015, 52, 147–158. [Google Scholar] [CrossRef] [PubMed]
  16. Kozlowski, A.J.; Bryce, T.N.; Dijkers, M.P. Time and effort required by persons with spinal cord injury to learn to use a powered exoskeleton for assisted walking. Top. Spinal Cord Inj. Rehabil. 2015, 21, 110–121. [Google Scholar] [CrossRef] [PubMed]
  17. Escalona, M.J.; Brosseau, R.; Vermette, M.; Comtois, A.S.; Duclos, C.; Aubertin-Leheudre, M.; Gagnon, D.H. Cardiorespiratory demand and rate of perceived exertion during overground walking with a robotic exoskeleton in long-term manual wheelchair users with chronic spinal cord injury: A cross-sectional study. Ann. Phys. Rehabil. Med. 2018, 61, 215–223. [Google Scholar] [CrossRef]
  18. Kressler, J.; Thomas, C.K.; Field-Fote, E.C.; Sanchez, J.; Widerstrom-Noga, E.; Cilien, D.C.; Gant, K.; Ginnety, K.; Gonzalez, H.; Martinez, A.; et al. Understanding therapeutic benefits of overground bionic ambulation: Exploratory case series in persons with chronic, complete spinal cord injury. Arch. Phys. Med. Rehabil. 2014, 95, 1878–1887.e4. [Google Scholar] [CrossRef]
  19. Duddy, D.; Doherty, R.; Connolly, J.; McNally, S.; Loughrey, J.; Faulkner, M. The effects of powered exoskeleton gait training on cardiovascular function and gait performance: A systematic review. Sensors 2021, 21, 3207. [Google Scholar] [CrossRef]
  20. Jang, Y.C.; Park, H.K.; Han, J.Y.; Choi, I.S.; Song, M.K. Cardiopulmonary function after robotic exoskeleton-assisted over-ground walking training of a patient with an incomplete spinal cord injury: Case report. Medicine 2019, 98, e18286. [Google Scholar] [CrossRef]
  21. Kim, H.S.; Park, J.H.; Lee, H.S.; Lee, J.Y.; Jung, J.W.; Park, S.B.; Hyun, D.J.; Park, S.; Yoon, J.; Lim, H.; et al. Effects of wearable powered exoskeletal training on functional mobility, physiological health and quality of life in non-ambulatory spinal cord injury patients. J. Korean Med. Sci. 2021, 36, e80. [Google Scholar] [CrossRef]
  22. US Food and Drug Administration. Investigational Device Exemptions (IDEs) for Early Feasibility Medical Device Clinical Studies, Including Certain First in Human (FIH) Studies; US Food and Drug Administration: Rockville, MD, USA, 2013; pp. 1–40.
  23. Hyun, D.J.; Lim, H.; Park, S.; Yoon, J.; Jung, K.; Bae, K.; Lee, I. Walking propulsion generation in double stance by powered exoskeleton for paraplegics. Robot. Auton. Syst. 2019, 116, 24–37. [Google Scholar] [CrossRef]
  24. Bohannon, R.W.; Crouch, R. Minimal clinically important difference for change in 6-minute walk test distance of adults with pathology: A systematic review. J. Eval. Clin. Pract. 2017, 23, 377–381. [Google Scholar] [CrossRef] [PubMed]
  25. Macfarlane, D.J.; Wong, P. Validity, reliability and stability of the portable Cortex Metamax 3B gas analysis system. Eur. J. Appl. Physiol. 2012, 112, 2539–2547. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Karvonen, J.; Vuorimaa, T. Heart rate and exercise intensity during sports activities. Practical application. Sports Med. 1988, 5, 303–311. [Google Scholar] [CrossRef]
  27. Collins, E.G.; Gater, D.; Kiratli, J.; Butler, J.; Hanson, K.; Langbein, W.E. Energy cost of physical activities in persons with spinal cord injury. Med. Sci. Sports Exerc. 2010, 42, 691–700. [Google Scholar] [CrossRef]
  28. Garber, C.E.; Blissmer, B.; Deschenes, M.R.; Franklin, B.A.; Lamonte, M.J.; Lee, I.M.; Nieman, D.C.; Swain, D.P. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: Guidance for prescribing exercise. Med. Sci. Sports Exerc. 2011, 43, 1334–1359. [Google Scholar] [CrossRef]
  29. Lewis, J.E.; Nash, M.S.; Hamm, L.F.; Martins, S.C.; Groah, S.L. The relationship between perceived exertion and physiologic indicators of stress during graded arm exercise in persons with spinal cord injuries. Arch. Phys. Med. Rehabil. 2007, 88, 1205–1211. [Google Scholar] [CrossRef]
  30. Ravensbergen, H.J.; de Groot, S.; Post, M.W.; Slootman, H.J.; van der Woude, L.H.; Claydon, V.E. Cardiovascular function after spinal cord injury: Prevalence and progression of dysfunction during inpatient rehabilitation and 5 years following discharge. Neurorehabilit. Neural Repair 2014, 28, 219–229. [Google Scholar] [CrossRef] [Green Version]
  31. Policarpo, F.; Valdivia-Moral, P.; Luna-Cruz, M.d.S.; Véliz-Burgos, A.; Mansilla-Sepulveda, J.; Estay-Sepulveda, J.G. Comparison between different prescription methods for aerobic training in young adults. Sustainability 2019, 11, 6420. [Google Scholar] [CrossRef] [Green Version]
  32. Cifu, D.X. Braddom’s Physical Medicine and Rehabilitation, 5th ed.; Elsevier: Philadelphia, PA, USA, 2015. [Google Scholar]
  33. Rivera-Brown, A.M.; Frontera, W.R. Principles of exercise physiology: Responses to acute exercise and long-term adaptations to training. PM&R 2012, 4, 797–804. [Google Scholar] [CrossRef]
Figure 1. Exoskeleton-assisted overground walking with a portable gas analyzer.
Figure 1. Exoskeleton-assisted overground walking with a portable gas analyzer.
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Figure 2. Changes in exercise intensity measured according to the (a) peak and (b) average (avg) metabolic equivalent of tasks (METs) for persons with spinal cord injury, (c) peak and (d) average heart rate relative to the heart rate reserve (%HRR), and (e) O2 cost of walking measured using oxygen consumption (VO2avg in mL/kg/min) divided by walking speed (m/min) (O2walking).
Figure 2. Changes in exercise intensity measured according to the (a) peak and (b) average (avg) metabolic equivalent of tasks (METs) for persons with spinal cord injury, (c) peak and (d) average heart rate relative to the heart rate reserve (%HRR), and (e) O2 cost of walking measured using oxygen consumption (VO2avg in mL/kg/min) divided by walking speed (m/min) (O2walking).
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Table 1. Demographic and clinical characteristics of the participants.
Table 1. Demographic and clinical characteristics of the participants.
NoSexAge (yrs)Height (cm)Weight (kg)Time Since Injury (yrs)NLIAISL/E Motor Score
1M5217172.92.9T10A0
2M4618075.64.8T8A0
3M3517577.83.6T10A0
4F58163757.9C6C12
5M491616215.6T10A0
6M49167743.5T11A0
7F4617064.94T10A2
8F351605212.1L1A0
9M6316471.41.1T4C15
10M4817270.11.3T1B0
Mean ± SD 48.1 ± 8.7168.3 ± 6.569.6 ± 7.95.7 ± 4.8
Abbreviations: yrs = years, BMI = body mass index, NLI = neurologic level of injury, AIS = American Spinal Injury Association impairment scale, L/E = lower extremity, M = male, F = female, SD = standard deviation.
Table 2. Walking distance in the 6-min walk test and cardiorespiratory outcome measures.
Table 2. Walking distance in the 6-min walk test and cardiorespiratory outcome measures.
Pre-TrainingMid-TrainingPost-TrainingPre- vs. Mid-Pre- vs. Post-Mid- vs. Post-
Total distance (m)20.7 ± 5.537.5 ± 10.549.1 ± 15.20.0050.0050.014
VO2rest (mL/kg/min)3.6 ± 0.73.7 ± 1.03.2 ± 0.90.8590.2410.261
VO2peak (mL/kg/min)13.8 ± 3.413.2 ± 2.013.3 ± 3.30.9990.7990.838
VO2avg (mL/kg/min)8.8 ± 2.59.5 ± 1.59.4 ± 1.90.2620.4440.610
HRrest (bpm)84.0 ± 10.382.3 ± 9.077.7 ± 8.90.7220.1830.032
HRpeak (bpm)121.1 ± 20.5118.6 ± 13.6115.7 ± 27.70.6090.2840.074
HRavg (bpm)111.5 ± 17.2110.0 ± 11.7100.3 ± 10.70.7210.0280.009
Abbreviations: VO2 = oxygen consumption, avg = average, HR = heart rate, bpm = beat per minute; Values are mean ± standard deviation.
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Park, J.H.; Kim, H.S.; Jang, S.H.; Hyun, D.J.; Park, S.I.; Yoon, J.; Lim, H.; Kim, M.J. Cardiorespiratory Responses to 10 Weeks of Exoskeleton-Assisted Overground Walking Training in Chronic Nonambulatory Patients with Spinal Cord Injury. Sensors 2021, 21, 5022. https://0-doi-org.brum.beds.ac.uk/10.3390/s21155022

AMA Style

Park JH, Kim HS, Jang SH, Hyun DJ, Park SI, Yoon J, Lim H, Kim MJ. Cardiorespiratory Responses to 10 Weeks of Exoskeleton-Assisted Overground Walking Training in Chronic Nonambulatory Patients with Spinal Cord Injury. Sensors. 2021; 21(15):5022. https://0-doi-org.brum.beds.ac.uk/10.3390/s21155022

Chicago/Turabian Style

Park, Jae Hyeon, Hyeon Seong Kim, Seong Ho Jang, Dong Jin Hyun, Sang In Park, JuYoung Yoon, Hyunseop Lim, and Mi Jung Kim. 2021. "Cardiorespiratory Responses to 10 Weeks of Exoskeleton-Assisted Overground Walking Training in Chronic Nonambulatory Patients with Spinal Cord Injury" Sensors 21, no. 15: 5022. https://0-doi-org.brum.beds.ac.uk/10.3390/s21155022

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