Key Points
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Using a robotic exoskeleton for exoskeleton-assisted walking has improved quality of life and mental health for individuals with spinal cord injury according to self-report measures.
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For individuals living with spinal cord injury, adding exoskeleton-assisted walking to rehabilitation has translated to improvements in motor and autonomic function.
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Robotic exoskeletons are a feasible approach to enhance task-specific training for locomotion.
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In animal and human trials, a robotic exoskeleton has demonstrated efficacy as a stand-alone intervention and in combination with other neuromodulatory approaches to enhance neuroplasticity.
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These positive changes in neuroplasticity (e.g., improved neural connectivity) due to exoskeleton-assisted walking have been demonstrated in several clinical populations (e.g., stroke, muscular dystrophy) with improved outcome measures, such as gait speed.
Overground locomotion is a dream goal for more than a million survivors with spinal cord injury (SCI). Today, advances in medical research findings through tissue engineering, stem cell research, and the development of neuroprostheses have paved the scientific road to achieve this goal. A key neurophysiological principle that has evolved over the last 3 to 4 decades and strengthened these findings is that task-specific training is highly important to restore standing and stepping in persons with SCI. Task-specific training relies on repetitively administering afferent influx to the nervous system to modulate specific behavioral or functional motor output. This volley of afferent influx is likely to be integrated at the central pattern generators to generate a pattern of flexion-extension oscillation (i.e., fictive locomotion) and ultimately result in a motor behavior similar to walking. Lovely et al. were among the first to demonstrate the effects of task-specific training on cats with completely transected cords (T12–T13). After 5 to 7 months of training, the paralyzed cats were capable of full weight-bearing and regained control of hind limb stepping.
Task-specific training resulting in neuroplastic adaptations of the injured spinal cord has emerged as a potential rehabilitation intervention that may restore overground locomotion in persons with SCI. Neuroplastic pathways may effectively integrate neural, neurochemical, metabolic, and muscular systems to enhance functional adaptions after SCI. In 2006, Dobkin et al. published the first multicenter randomized clinical trial that demonstrated the efficacy of task-specific training on overground mobility in persons with incomplete SCI. The authors implemented body weight supported treadmill training (BWSTT) for 12 weeks and compared it to overground training. The findings suggested that task-specific training using either BWSTT or overground ambulation is equally effective in the rehabilitation of persons with incomplete SCI.
These outcomes intrigued several other groups, causing them to explore the effects of task-specific training on restoring overground locomotion in persons with SCI. This has sequentially resulted in the development of the Reeve Foundations NeuroRecovery Network clinical centers that deliver extensive rehabilitation for persons with SCI. The NeuroRecovery Network provides locomotor training combined with functional electrical stimulation (FES) to enhance motor recovery after SCI. The goal of the program is to provide continuous training to enhance neuroplasticity of the injured cord.
Recently, the robotic exoskeleton has emerged as a potential successful rehabilitation tool that can provide immediate overground ambulation for persons with SCI. An introductory editorial suggested that robotic exoskeletons encompass the future of rehabilitation in persons with SCI. Several exoskeleton devices have been developed to allow overground stepping with varying efforts, including some that are approved by the Food and Drug Administration, such as, the ReWalk, Indego, Ekso Bionics, and others that remain experimental. Unlike strenuous task-specific training, robotic exoskeleton ambulation does not require the same number of trained staff that are typically involved in BWSTT. It is common to have three or four therapists involved in the training of one person during BWSTT compared with only one or two therapists when using the exoskeleton for overground ambulation. We have previously contrasted different brands of exoskeletons and highlighted the potential indications for each brand after SCI. A thematic review also has detailed several of the pros and cons that need to be considered when prescribing robotic exoskeletons for the rehabilitation of persons with SCI. The purpose of this chapter is (1) to review recent accomplishments in the applications of robotic exoskeletons for the rehabilitation of persons with neurologic disabilities and (2) to develop the hypothesis that robotic exoskeletons can be used as an effective neuroprosthesis for task-specific training in persons with SCI. This is important because several research investigators are still debating the efficacy of the robotic exoskeleton to enhance neuroplasticity and to facilitate overground ambulation.
Definition of Lower Limb Robotic Exoskeleton
For the purpose of this chapter, a lower limb robotic exoskeleton or exoskeleton-assisted walking (EAW) will be defined as a computerized unit that involves sensors, actuators, algorithms, a structural framework, and control strategies capable of processing information to execute functional movements. The structural framework involves external robotic legs joined at the hip and knee joints and pelvic-hip support with or without trunk support. Furthermore, the robotic exoskeleton field has increased to involve rehabilitation of the upper extremities, trunk control, balance, lower extremity training, and gait reeducation. In this chapter, we are going to focus on gait reeducation in persons with neurologic disabilities and primarily persons with SCI ( Table 7.1 ). We should also point the reader’s attention to another Chapter 33 that was dedicated for a similar purpose.
| Indication | Benefits of USING EAW |
|---|---|
| Physical activity—locomotion | |
| Pulmonary function |
|
| Lower extremity motor function |
|
| Seated balance |
|
| Spasticity |
|
| Bowel function |
|
* Benefits noted for individuals with SCI and stroke; all other benefits apply to SCI only.
Major Indications and Accomplishments of Robotic Exoskeletons
Exoskeleton and Quality of Life
A current multicenter cooperative study has furnished the road to investigate the effects of the robotic exoskeleton on quality of life (QOL) and other comorbidities after SCI. Preliminary evidence indicated that EAW remarkably enhanced QOL and increased independence in persons with SCI. Although the trial was limited to one brand of robotic exoskeleton and only targeted veterans with SCI, striding benefits have been inferred from the trial that will shape future rehabilitation programs and enhance our understanding of the design of future exoskeletons and the interface between humans with physical disabilities and robotics.
Earlier studies have also taken a cursory look at QOL for individuals living with SCI using subjective outcome measures. In a pre-post study including 45 participants, there was a slight increase in the Satisfaction with Life Scale; however, this increase was not significant. Despite these findings, Juszczak et al. observed that some participants had the potential to operate an exoskeleton in the community thus facilitating increased participation and theoretically altering QOL. In one case study, an individual living with SCI noted that using an exoskeleton had a positive effect on QOL as shown by significant improvements in six out of eight thematic areas of the Short Form 36 Health Survey.
A Canadian study provided home use of robotic EAW for the purpose of indoor exercise and outdoor activities. Fourteen participants with SCI were asked to complete the Dutch version of the Quebec User Evaluation of Satisfaction With Assistive Technology scale (1–5 scale) and the System Usability Scale (0–100 scale) questionnaires at the beginning and at the end of a 2- to 3-week period. Participants reported that EAW was used for individual exercise for 74% of all sessions and for 48% of outdoor activities. The Quebec User Evaluation of Satisfaction With Assistive Technology scale showed dissatisfaction regarding the weight of the exoskeleton, ease of use, and safety. The participants reported mixed signs of positive (mental health [n = 5], decreased spasticity [n = 3], neuropathic pain [n = 1] and increased range of motion [n = 1]) and negative (muscle or joint pain [n = 1], skin damage [n = 2], increased spasticity [n = 1] and fecal incontinence problems [n = 1]) health outcomes.
Exoskeleton and Physical Activity
The first observation showed that using a robotic exoskeleton resulted in a 30% increase in walking speed after longitudinal training of eight individuals with SCI. This study showed a reduction in temporal parameters including stride time, stance time, and double-support time. The findings may suggest enhancement of the motor learning curve after more than 100 hours of EAW.
Another case report noted that the level of physical activity increased in a participant with C4 complete SCI. The participant, using a platform roller walker, demonstrated that both standing time and walking time increased within two sessions. These findings may collectively suggest that despite the level of injury and severity of injury, EAW may be capable of increasing the level of physical activity in persons with SCI. Anecdotally, most participants with SCI reported enjoyment of the training session and trained up to 120 minutes without reporting any signs of fatigue. This anecdotal evidence may support earlier findings that noted reduced metabolic cost during robotic training and may explain the lower rate of fatigue during EAW compared with other training modalities.
Exoskeleton and Pulmonary Function
Enhancement in the level of physical activity is also accompanied by increased oxygen uptake. A recent study demonstrated that 60 sessions of EAW resulted in increased gait speed by 94%, decreased rate of perceived exertion by 46%, and increased VO 2 by 30%. Another recent study from our laboratory showed that following 12 weeks of exoskeleton training, twice weekly, there was no effect on peak VO 2 . Compared with resting sitting and resting standing, VO 2 increased 2 and 1.11 times during EAW, respectively. These findings were previously confirmed in two different studies using other brands of exoskeletons. However, in a recent study, EAW training also showed a decrease in peak VO 2 by 17%. In a case report, the authors noted no difference in 6-minute VO 2 when using Canadian crutches compared with a standard roller walker.
In a randomized controlled pilot study, Xiang et al. found that EAW positively affected pulmonary function in individuals living with SCI. Participants underwent 1 hour of EAW training or conventional training (i.e., strength and aerobic exercise) 4 days per week for a total of 4 weeks (16 sessions). After training, the EAW group showed significantly higher values of forced vital capacity (FVC) (3.8 ± 1.1 L) predicted FVC% (94.1% ± 24.5%) and forced expiratory volume in 1 second (FEV 1 ) (3.5 ± 1.0 L) in comparison with the conventional group (FVC: 2.8 ± 0.8 L; FVC% predicted = 65.4% ± 17.6%; FEV 1 : 2.4 ± 0.6 L). Similar to the findings by Knezevic et al. and Sutor et al., these results show that EAW has the potential to improve pulmonary function in individuals with SCI.
Exoskeleton and Lower Extremity Motor Function
Another pilot study clearly demonstrated that EAW enhanced motor function in persons with acute SCI. The study showed lower extremity motor scores and the Functional Independence Measure increased 3.1 and 1.4 times, respectively, more than controls who did not undergo EAW. These findings were confirmed in a multicenter trial that showed that 36 sessions of EAW resulted in 80%, 82%, and 84% completion of the 10-m walking time (10-MWT; ≤40 seconds), distance during 6-minute walking time (6-MWT; ≥80 m), and time up to go (≤90 seconds) criteria. A similar observation was noted in 50 participants with a stroke who completed single-blinded randomized parallel trial for 6 to 8 weeks. EAW resulted in improvement in walking speed (0.24 m/s), walking endurance (11%), balance (17.9%), and corticomotor excitability (145%) compared with controls in persons with hemorrhagic stroke.
An observational study with 28 participants with SCI also showed positive improvements in gait parameters. Over 2 weeks (10 sessions) there was an increase in participants’ walking speed during the 10-MWT (≥0.03 m/s) and distance during the 6-MWT (≥11 m) while wearing the exoskeleton. Interestingly, individuals with complete injuries ASIA Impairment Scale (AIS A) showed more improvement in both gait speed and distance than those classified as AIS B. The same findings were true for individuals with higher injuries compared with those with lower injuries. Unfortunately, there was no improvement in lower extremity motor scores across participants; however, in a study by Aach et al., lower extremity motor scores improved significantly (21.75 ± 8.3 to 24.38 ± 7.6) in all participants with chronic SCI (n = 8) in addition to an increase in leg circumference (5–50 mm) in seven participants and a reduction in leg circumference (25 mm) due to edema in the remaining participant.
Nine participants with stroke were enrolled in a quasicontrolled trial with 12 weeks of twice weekly therapy using the REX exoskeleton (Auckland, New Zealand). The primary outcomes were measured by using the five-item motor assessment scale. The five-item scale includes supine to side lying, supine to sitting, balanced sitting, sitting to standing, and walking. Other batteries of motor outcomes were included. Overall, there was no change in motor function; however, five out of the nine participants had changes that indicated improvements in their motor scores. Four out of these five participants had the lowest motor scores at the time of enrollment in the study. Other improvements were observed in the grip strength of the affected limb, the electromyography of the affected quadriceps, and independence with activities of daily living. These findings suggest that EAW may result in both spinal and cortical neuroplasticity that act to improve functional outcomes.
Exoskeleton and Seated Balance
Developing effective training strategies, such as using a robotic exoskeleton to reactivate trunk muscles, are needed to facilitate independence during seated balance activities in individuals with SCI. In a pilot study, Tsai et al. showed that EAW training transferred to improvements in seated balance for eight individuals with SCI. After a median of 30 (range 7–90) sessions, a significant improvement was found in endpoint excursion and maximal excursion. Median endpoint excursion scores increased from 37.2 to 48.7, and median maximal excursion scores increased from 58.0 to 78.3. Other improvements were noted in the modified Functional Reach Test and subscales of physical functioning and role limitations; however, these improvements were not significant.
Furthermore, a case report by Chisholm et al. showed that overground compared with stationary (i.e., treadmill) EAW produced a larger improvement in postural stability. Three individuals with motor complete SCI underwent 30 sessions of robotic gait training. They completed a randomized trial using one of two alternating treatment designs beginning with either a stationary or an overground EAW intervention. Results showed that overground EAW actively recruited trunk muscles through postural control mechanisms. Although both groups showed improved seated balance control, as evidenced by reduced time taken during the T-Shirt Test and increased distance on the modified Functional Reach Test, the overground group improved slightly more than the stationary EAW group.
Exoskeleton and Indices of Spasticity
Frequency and severity of spasticity have been positively affected though overground EAW. In a pre-post study by Stampacchia et al., 21 individuals with SCI showed improvements in spasticity after completing only one overground walking session using a powered exoskeleton. The session lasted 40 minutes with 7 to 25 minutes of active walking time. Participants subjectively evaluated perceived spasticity using a 0- to 10-point numerical rating scale. Using this scale, the median score decreased from 2.0 to 0.0 after the walking session. Objective assessments of spasticity were measured using the Modified Ashworth Scale (MAS) and the Penn Spasm Frequency Scale (PSFS). Scores on these scales improved from a median score of 4.0 to 2.0 on the MAS and 1.0 to 0.0 on the PSFS.
Another pre-post intervention, across five rehabilitation institutes, showed mostly positive effects of EAW on spasticity. Forty-five participants living with SCI engaged in three to four EAW sessions per week for 8 weeks, completing a total of 26 sessions. These individuals reported a significant reduction in spasticity from the start (1.6 ± 0.9) to the end of the study (0.9 ± 1.7). Although most participants experienced a decrease (n = 12) or no change (n = 28) in spasticity, as evidenced by the MAS, few participants’ (n = 5) spasticity increased.
Exoskeleton and Bowel Function
An observational study noted improvements in bowel function following 25 to 63 sessions of EAW. Participants (50%–80%) reported an improvement in the frequency of the bowel evacuations, fewer bowel accidents, reduced laxative and stool softener use, and improved overall satisfaction and related QOL. The reduction in the use of laxative and stool softener is considered important finding because they negatively impact the beneficial gut microbiome. The disruption in gut microbiome is likely to increase the risks of other comorbidities including obesity, insulin resistance, and type II diabetes in persons with SCI. The findings were just recently confirmed in a randomized controlled trial that demonstrated that EAW plays a major role in overcoming bowel dysfunction in persons with SCI. The time to complete bowel management decreased in 24% of the EAW participants in this study.
Exoskeleton as a Platform for Neuromodulation Techniques to Enhance Neuroplasticity
Growing evidence suggests that robotic exoskeletons can be used as a neuroprosthesis for sensorimotor rehabilitation in persons with SCI. Several animal and human trials have demonstrated the efficacy of robotic exoskeleton use in conjunction with neuromodulatory approaches such as trans-spinal stimulation (TS) or implanted epidural stimulation (ES) as well as brain-computer interfaces. A brain-computer interface integrates the user’s volitional intention with the operation of a robotic exoskeleton. It has the potential to achieve this integration between devices in persons with different neuromotor disorders. Myoelectric control is another example of using either electromyography to control exoskeleton ambulation or integrating FES with a robotic exoskeleton. A previous editorial described the combinatory approach of EAW with neuromodulation techniques as promising for gait rehabilitation in persons with SCI. This integrative approach provides the opportunity to augment the automaticity of the spinal circuitries to enhance volitional stepping. Eventually, it can be translated into overground locomotion in persons with SCI. Furthermore, it provides sensorimotor integration of the spinal and supraspinal networks.
Although the major focus of these studies was to provide an alternative approach for task-specific training, there remains an important question of whether EAW can be used as an alternative to the labor-intense BWSTT approach. EAW has been recognized as an effective approach to enhance neuroplasticity. EAW is characterized by a lower metabolic cost and enhancement of QOL and has the capability to offer full overground weight-bearing on day one in completely paralyzed persons with SCI. Multiple studies have demonstrated improvement in electromyography activities of the paralyzed muscles following EAW training in persons with SCI. In this section, we are going to review the evidence that may support developing the hypothesis that EAW can be used for enhancing neuroplasticity after SCI. We will start with animal studies and then follow with human trials.
In the journal Science , van den Brand et al. showed that a robotic postural interface combined with ES resulted in recovery of voluntary movements in completely transected rats. Using both paradigms, rats were capable of initiating and sustaining full weight-bearing bipedal locomotion following daily training for 30 minutes for 5 to 6 weeks. The authors suggested that this multisystem neuroprosthetic training resulted in the formation of intraspinal detours that relay supraspinal information. This was accompanied by an increase in the number of neurons after continuous locomotion in the overground trained rats compared with the nontrained rats. This paradigm of combining a robotic interface with ES has been adopted in number of other research studies that were conducted by the same group.
Gad et al. demonstrated that combining EAW with noninvasive TS resulted in positive synergistic effects as demonstrated by increasing the effort of walking, interlimb coordination, and smoothened stepping in a person SCI. In this case report, an individual with motor complete SCI completed overground stepping using an exoskeleton enhanced with TS and/or a pharmacologic intervention (i.e., buspirone). Using the exoskeleton, after overground baseline training for 4 weeks, the participant engaged in 1 week of training using TS only followed by 1 week using the drug therapy only. The last week of stepping training combined TS and drug therapy. Sessions took place 5 days per week for 1 hour using the variable assist mode. When used, noninvasive TS was delivered at the spinous process between T11 and T12 and at a frequency of 30 Hz. Average subjective scores on the participant’s perception of improved muscle tone, sensation, early morning sensation, body perspiration, and hand-to-leg coordination were highest in the TS only and TS + drug conditions. The TS-only condition reduced mean step cycle duration from 2.13 seconds to 2.03 seconds and 2.07 seconds in the drug-only condition. The mean step cycle duration decreased the most in TS + drug condition (2.00 seconds). Higher levels of assistance from the exoskeleton were needed when TS was not present. Delivering assistance as needed resulted in the participant engaging the lumbosacral spinal networks to control the swing phase in one leg while the opposite leg remained in stance. The use of TS with EAW resulted in a remarkable decrease in the provided robotic assistance and an increase in the integrated activities of rectus femoris and tibialis anterior muscles. TS also supported the stimulation of standing and stepping through modulating the excitability of the spinal neural networks to reestablish connections from cortical networks to spinal networks. Thus, a high level of agonist-antagonist coordination was established through these highly excitable network projections to the motor pools. Furthermore, the variable assist mode in this study provided an opportunity to engage the central pattern generators to initiate stepping during the swing phase when TS pulses were delivered. These findings were recently confirmed in three persons with chronic complete SCI when TS was combined with EAW for 12 weeks. The authors noted an increase in the amplitude of the knee extensors after using TS with EAW compared with EAW only both at the stance and the swing phased of the gait cycle. The amplitude of the extensor muscle was still enhanced even when lowering the assistance provided with EAW. Two of the three participants showed a considerable reduction in the robotic assistance needed during EAW with the use of TS.
Similar to TS, the addition of ES to locomotor training alone has resulted in neuromodulation of the spinal cord circuitries in individuals with SCI. These preliminary findings indicated successful overground stepping and walking in persons with complete SCI. In a case report, Gorgey et al. found that using ES combined with EAW improved motor control during stepping in an individual with a complete SCI. This participant underwent 24 sessions of EAW over 12 weeks. As EAW assistance decreased (100% to 35%), the ratio of walk time to stand time increased (0.77–0.86). Electromyography patterns revealed accompanying improvements in lower extremity motor function. Clearly, these results demonstrated improvements in motor control; however, these improvements only occurred while ES was on.
A randomized clinical trial suggested that powered EAW may improve gait recovery by shaping the neuroplasticity of specific brain centers. After enrolling 40 participants with stroke into either EAW plus overground training (n = 20) or only overground training (n = 20) for 8 weeks, individuals were evaluated on their gait performance (10-MWT), gait cycle, and muscle activation pattern using electromyography. Neural connectivity was evaluated using transcranial magnetic pulses to evoke motor potentials at the relaxed abductor hallucis muscle, conditioning electrical stimulation of the big toe as well as high-input EEG unit. Both groups showed improvement in the10-MWT and the Rivermead Mobility Index as well as a reduced Timed Up and Go (TUG) Test; however, the overall improvement was greater in the EAW plus overground training group compared to the overground training only group.
The use of EAW to enhance neuroplasticity and subsequently motor recovery has expanded to other clinical populations with different neuromuscular disorders. One study demonstrated that the use of the HAL exoskeleton in conjunction with treadmill training enhanced 10-MWT, 6-MWT, and TUG Test following 8 weeks in limb-girdle muscular dystrophy patients. In two people with SCI with severe spasticity, peroneal nerve stimulation was used to stimulate flexor withdrawal reflex to suppress the extensor tone during swing phase with EAW. This facilitated hip flexion and knee flexion during the gait cycle. The two subjects had difficulty performing toe-off during the swing phase prior to applications of peroneal nerve stimulation. Hybrid technologies have been developed combining FES and exoskeleton (i.e., FEXO) to facilitate neurorehabilitation. However, the integration of these two different technologies is challenging as far as timing, and they require a closed-loop system (i.e., feedforward control of FES and feedback control of the exoskeleton) to ensure harmonic movements. This hybrid technology provides a successful marriage of FES and the exoskeleton to overcome several of the caveats of using each system separately. For example, FES results in excessive muscle fatigue and is unlikely to promote walking for a long distance in persons with SCI. In healthy and paralyzed individuals, the integration of the FEXO Knee system was successful in enhancing the rhythmicity of central pattern generators and promoting torque production for effective movement. The use of the knee exoskeleton compensated for insufficient torque production and detected torque error during FES to induce leg flexion and extension.
In summary, EAW shows promise to improve different activities, functions, and QOL for individuals living with SCI and other neurologic conditions. The addition of EAW to rehabilitation programs for individuals living with paralysis can translate to potential improvements in physical activity (i.e., locomotion), pulmonary function, lower extremity motor function, seated balance, spasticity, and bowel function. BWSTT provides similar benefits for individuals with neurologic conditions; however, it appears that the addition of a robotic exoskeleton to therapy sessions may be more feasible. Other neuromodulatory methods have also been used in addition to the robotic exoskeleton in both animal and human studies. The findings from these studies suggest that EAW is an effective task-specific modality for the enhancement of overground locomotion in persons with neurologic disabilities. Robotic exoskeletons offer a feasible platform to combine with other neuromodulatory approaches that may facilitate integration of spinal and supraspinal neural controls to enhance motor recovery following neurologic disorders. This combination offers a selection of multimodal rehabilitation interventions that promote neuroplasticity at different levels and ensures widespread, safe practice in clinical settings.
References
Related posts:
Introduction—The Growing Role of Robotics in Health Care
Robot and Artificial Intelligence Companies Around the Globe
Medical Robotics in Acute Care Medicine (Urgent Care, Pain Management, and Robot-Assisted Surgery)
Robots on the Battlefield and for Space Travel
Brain-Controlled Assistive Robotics and Prosthetics
The Future of Robots in Medicine
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