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Article

Can Robotic Therapy Improve Performance in Activities of Daily Living? A Randomized Controlled Trial in Sub-Acute Spinal Cord Injured Patients

by
Vicente Lozano-Berrio
1,
Mónica Alcobendas-Maestro
2,
Raquel Perales-Gómez
3,
Yolanda Pérez-Borrego
4,
Angel Gil-Agudo
1,2,5,
Begoña Polonio-López
6,
Camilo Cortés
7 and
Ana de los Reyes-Guzmán
1,5,*
1
Biomechanics and Technical Aids Unit, Hospital Nacional de Parapléjicos (SESCAM), 45004 Toledo, Spain
2
Rehabilitation Department, Hospital Nacional de Parapléjicos (SESCAM), 45004 Toledo, Spain
3
Occupational Therapy Unit, Hospital Nacional de Parapléjicos (SESCAM), 45004 Toledo, Spain
4
Functional Exploration and Neuromodulation of Nervous System Investigation Group, Hospital Nacional de Parapléjicos (SESCAM), 45004 Toledo, Spain
5
Unidad de Neurorrehabilitación, Biomecánica y Función Sensitivo-Motora (HNP-SESCAM), Unidad Asociada I+D+I al CSIC, 45071 Toledo, Spain
6
Technological Innovation Applied to Health Research Group (ITAS), Faculty of Health Sciences, University of Castilla-La Mancha, 45600 Talavera de la Reina, Spain
7
Digital Health and Biomedical Technologies, Vicomtech Foundation, Basque Research and Technology Alliance (BRTA), 20014 Donostia-San Sebastián, Spain
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(18), 8478; https://doi.org/10.3390/app14188478
Submission received: 12 August 2024 / Revised: 9 September 2024 / Accepted: 18 September 2024 / Published: 20 September 2024
(This article belongs to the Special Issue Current Status and Perspectives in Physical and Rehabilitation Medicine)
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Abstract

:
(1) Background: The influence of robotic therapy on patients with sub-acute cervical spinal cord injury (SCI) for improving their activities of daily living (ADL) performance is unclear; (2) Methods: 31 subjects with cervical SCI completed the training randomly assigned to an intervention or control group during 40 sessions. All the subjects received, in each session, 30 min of upper-extremity conventional therapy. In addition, the subjects within the control group received another 30 min of conventional therapy, whereas subjects within the intervention group received 30 min of robotic therapy with Armeo Spring (Hocoma AG, Volketswil, Switzerland). Therefore, the ADL of drinking was trained by using the exoskeleton. Feasibility and efficacy measurements as clinical scales and kinematic indices, and usability questionnaires, were used as assessment at baseline and at the ending of the study (week 10); (3) Results: The intervention group significantly improved with regards to the feeding and grooming items of the Spinal Cord Independence Measure scale. The improvement in the movement smoothness related to the activity of drinking was greater in the intervention group than in the control (p = 0.034); (4) Conclusions: The findings of this study reveal that patients with cervical SCI improve their performance in ADL with robotic therapy.

1. Introduction

The clinical expression of cervical spinal cord injury (SCI) and, therefore, the impairments of the upper extremity (UE) function, is highly variable depending on the level and severity (complete versus incomplete, depending on the extent of sensorimotor preservation below the injury level) [1,2]. However, patients with complete SCI can voluntarily activate paralyzed muscles alone or by engaging non-paralyzed muscles during neurophysiological assessments, indicating the presence of residual pathways across the injury. These phenomena have been researched for the UE muscles after cervical SCI, finding functional activity in clinically paralyzed muscles and indicating presence of residual pathways across the injury. This should be taken into account when designing rehabilitation therapies with the aim of promoting the strengthening of these residual connections [2].
Among the most devastating effects of cervical injuries is the loss of hand function [3]. UE function is considered one of the determining factors for independence in basic activities of daily living (ADL), as well as social and work activities [4]. Regaining partial function could lead to a higher independence level and, as a consequence, improve patients’ quality of life. Anderson et al. analyzed what functions were the most important to SCI patients in order to enhance their quality of life. As a result of a study performed on a sample of 681 SCI patients, regaining arm and hand function was the most important factor to patients with cervical SCI, whereas regaining the sexual function was the most important option for patients with paraplegia [5].
Recovery after SCI is a complex process that depends on different factors such as the severity and level of the injury, the medical and surgical care received after the injury, and the rehabilitation treatment [6].
On the one hand, recent advances in understanding the plasticity within the sensorimotor system have contributed to the development of novel non-invasive neurostimulation techniques in order to facilitate and promote UE motor recovery after SCI. One of these techniques is spinal cord transcutaneous stimulation for which UE neuromotor control, the recovery mechanisms, and the future directions of this field of research have been studied [7].
On the other hand, there is great interest in exploring novel rehabilitation technologies to augment conventional therapies to reduce neurological disability and improve patients’ function [8]. Robotic rehabilitation devices have the potential to deliver high-intensity and reproducible therapy [9], improving treatment adherence by using it in conjunction with virtual reality applications and obtaining objective and accurate kinematic information on quality, smoothness, motion deviation, and speed [10].
Due to the rapid growth in new technologies and devices over recent decades, there is an extensive variety of electromechanical devices for UE rehabilitation [11]. Due to the scientific collaborations that the Hospital Nacional de Parapléjicos has maintained with the Vicomtech technological center [12], Armeo® Spring (Hocoma AG, Switzerland) was the robotic device that was available to us to carry out this research. Specifically, the Armeo Spring robotic device has been previously applied in SCI populations [10,13] and other neurological pathologies such as stroke [14,15,16,17,18,19,20,21], cerebral palsy (CP) [22,23,24,25,26,27], and multiple sclerosis (MS) [28]. Scientific evidence in stroke populations concludes that it is not clear that UE therapy based on robotic devices (UE-RT) shown an improvement in the performance of basic ADL in stroke patients more than usual techniques or no treatment [29]. Previous studies in SCI populations lacked an independent control group as a comparator.
Taking this hypothesis as a starting point, the main objective of this study is to analyze the effectiveness of the Armeo Spring device for improving the performance of ADL. For this purpose, a virtual reality application based on the performance of the ADL of drinking from a glass using Armeo Spring has been developed and included within the UE-RT sessions conducted in this study. Therefore, as a novelty, in contrast with a previous study in subacute SCI subjects [13], an independent control group of subjects undergoing no Armeo Spring treatment was included and both the control and intervention groups were dose-matched; and assessments based on kinematic metrics from the performance of a biomechanical study have been included in the methodology. The secondary objectives of this study were to study the clinical feasibility of administering to patients for eight weeks a treatment based on UE-RT to complement the conventional therapy they receive; to analyze the influence of the emotional state of the patients in the study results; and to study the usability of robotic therapy.

2. Materials and Methods

2.1. Study Design and Randomization

This study was interventional, with a parallel assignment model, two arms, and randomized allocation into a control or intervention group by using sequentially numbered, opaque sealed envelopes. Then a computer-generated random numbers list and a researcher numbered the opaque sealed envelopes for use for the allocation. The random allocation sequence was generated by an external researcher in this study. Then, the participants were enrolled and assigned to interventions by clinical staff. The examiners were unaware of the experimental group assignment. Due to the clinical study being conducted within daily clinical practice, the subjects were randomized in blocks of 4 subjects. The study was registered with ClinicalTrials.gov (NCT04383873). The CONSORT flow chart is shown in Figure 1. The clinical trial ended when the study reached the scheduled date of closure.

2.2. Subjects

The recruitment was made with a total of 40 subjects with subacute cervical SCI from the inpatient population at Hospital Nacional de Parapléjicos between June 2016 and December 2021. The inclusion criteria were to have a cervical SCI above C8, be incomplete in the motor aspect or complete with areas of partial motor preservation at least C6, classified according to the International Standards for the Neurological Classification of Spinal Cord Injury (ASIA Impairment Scale (AIS)) [30] by the clinical personnel; have passed the critical phase after the injury, be in the active functional rehabilitation phase and have an evolution time of less than one year; be aged between 16 and 75 years old; have reached the seated posture and to be able to sign the corresponding written informed consent. The exclusion criteria were to have an unstable orthopaedic injury such as unconsolidated fractures or unstable osteosynthesis systems in UE; skin lesions and/or pressure ulcers in the exoskeleton placement area; joint stiffness and/or severe spasticity; bronchopneumopathy and/or severe heart disease that would require monitoring during the exercise; visual problems and cognitive impairment; and not signing the informed consent. The dominant hand of the patients was taken into account and assessed by means of Edinburg Handedness Inventory [31]. Five subjects were excluded for not meeting the inclusion criteria and another one declined to participate.

2.3. Robotic Device

The device used to carry out this study was Armeo Spring (Figure 2). Although it is a passive exoskeleton for UE rehabilitation, the possibility of compensating for the force of gravity on the arm and forearm levers allowed subjects with UE motor impairment that met the inclusion criteria to use it even in the early stages of their recovery. All the subjects began the UE-RT with the same gravity compensation level: B degree for the arm and A-B degree for the forearm. After the gravity compensation, the patient must have been able to hold their forearm actively in a horizontal position and their upper arm in a 45-degree flexion floating position with a minimal weight support.

2.4. Interventions

The study was organized with two groups: the intervention group and the control group. The treatment was unilateral. The choice of the UE treatment was made according to the rehabilitation objectives and by consulting with each subject.
The treatment was scheduled for 40 sessions, five one-hour UE therapy sessions per week for eight weeks (maximum 10 weeks). The sessions’ number was registered as a feasibility outcome and compliance. All the subjects received daily 30 min for 40 sessions of the treatment based on UE conventional therapy (UE-CT). In addition, subjects within the intervention group received daily 30 min sessions of using Armeo Spring device for 40 sessions. The both groups, intervention and control, were dose-matched, with the control group receiving an additional treatment based on UE-CT another daily 30 min for 40 sessions.
Each UE-RT session with Armeo Spring was divided into two parts: 15 min by means of virtual applications included in Armeo Spring software (Software Armeocontrol V1.21 and Armeo® Games V1.14) based on different modalities of reaching and grasping movements: Fruit Shopping, Window Mopping, Fish Catching, Egg Cracking, Shelf, and Reveal Picture were used in the daily UE-RT sessions; as well as 15 min with a virtual application designed specifically for rehabilitating the UE movement pattern related to the ADL of drinking. This virtual application was developed by Vicomtech technological center [12] based on guidelines from clinical staff (Figure 2). The developed application allows working, in addition to the reaching and grasping movement, and proximal movement towards the body. In this way, it is possible to conduct, by means of the UE-RT, a complete ADL simulating the performance of the real ADL of drinking from a glass. Therefore, the subjects within the control group could work, using the Armeo Spring, on the ADL movement pattern with the appropriate intensity and number of repetitions. Participants had no prior contact with the robotic device before the study began. Before starting the UE-RT sessions, a calibration session was conducted for each participant. In this session, the Armeo Spring was adapted to the anthropometric dimensions of each participant and the global workspace was set for each participant.
Each UE-CT session consisted of UE mobility and range of motion, and UE function and basic ADL with the assigned occupational therapist.
The placebo effect was resolved by offering subjects in the control group the possibility to undergo a few sessions of UE-RT after the study was completed.
The study was conducted according to the world Medical Association Declaration of Helsinki and the study protocol was approved by the local ethics committee (Comité Ético de Investigación Clínica, Complejo Hospitalario de Toledo; Approval number: 14/06/2016 (No. 85)).

2.5. Effectiveness Outcomes

The effectiveness of the Armeo Spring device in improving the performance of ADL was analyzed by means of these outcomes.
  • Upper Extremity Motor Score (UEMS) [30]. The UEMS consists of measurement of the strength of 5 key muscle groups in each UE between the range of 0 (absence of function) and 5 (normal function). In the present study, only the UEMS over the treated UE was taken into account, with a score range of between 0 and 25 points;
  • Spinal Cord Independence Measure (SCIM) [32]. The SCIM is a disability scale developed specifically for patients with spinal cord lesions in order to make the functional assessments of these patients more sensitive to changes. In this research, the self-care subscale and the total score were taken into account. A higher score corresponds to a higher degree of independence;
  • Capabilities of Upper Extremity (CUE) Questionnaire [33]. The CUE Questionnaire is a clinical scale designed to measure UE functional limitations in subjects with cervical SCI, representing the self-perceived difficulty in actions such as reaching or grasping. Therefore, the minimum score is 32 (worse UE function) and the maximum is 224 (complete UE function).
  • Jebsen-Taylor Hand Function (JTHF) [34]. The JTHF test was designed to provide a short, objective test of hand functions commonly used in ADL, specifically designed for a concrete pathology measuring the time in seconds of reaching each task. A higher spent time is a worse result;
  • Kinematic indices related for the ADL of drinking from a glass. Several kinematic indices were computed for characterizing the UL movement pattern during the performance of the drinking task in a real environment. Following the experimental protocol described in our previous study, the subjects were instrumented with the active markers of the photogrammetry system Codamotion (Charnwood Dynamics, Ltd., Rothley, UK) for measuring their UE kinematics during the performance of the drinking task in a real environment [35]. For each participant, this assessment was unilateral over the treated UL chosen in the context of this clinical study, analyzing the movement of the trunk, arm, forearm, and hand body segments. Then, the kinematic indices of accuracy, efficiency, agility, coordination, and smoothness were computed as measures of UE ability and dexterity [36,37]. Thus, accuracy and efficiency indices were computed from the hand trajectory during the movement; agility and smoothness indices from the analysis of the hand velocity profile; and coordination index from the joint kinematic data of the shoulder and elbow. The results related to the kinematic indices could be graphically expressed for each participant (Figure 3).
Moreover, as a measure of effectiveness, subjects’ evolution in terms of the gravity-compensation level in the Armeo Spring arm and forearm levers was registered.

2.6. Emotional State Outcomes

To assess the state of mood (anxiety and depression), two clinical scales were administered:
  • Hospital Anxiety and Depression (HAD) Scale [38]. The HAD Scale is a reliable instrument for screening clinically significant anxiety and depression in subjects universally across medical clinics. A score equal to or greater than 11 is considered as depression/anxiety. Between 0 and 7 is not considered depression/anxiety, and between 8 and 10 is a doubtful case;
  • Beck’s Depression Inventory (BDI) [39]. This depression inventory can be self-scored. The scoring scale is at the end of the questionnaire. The BDI consists of 21 items, giving a possible total of from 0 to 63 points. The interpretation of the score is as follows: from 0 to 10 points, these ups and downs are considered normal; from 11 to 16: slight disturbance of mood; from 17 to 20: intermittent states of depression; from 21 to 30: moderate depression; from 31 to 40: severe depression; and more than 40 points: extreme depression.

2.7. Usability Outcomes

The QUEBEC User’s Evaluation of Satisfaction with Assistive Technology (QUEST) was applied to subjects within the intervention group in relation to the UE-RT as a usability measure.
The subject questionnaire made use of a Likert scale. The scale previously used by other authors for subjects to provide feedback about their experience with the Armeo Spring device was used [13]. In this research, this scale introduces the novelty of two additional questions related to the ADL of drinking implemented within the Armeo Spring software. For each question, a score of 1 means ‘Disagree strongly’, a score of 7 means ‘Agree strongly’, and a score of 4 is ‘Neither agree nor disagree’.
The effectiveness measurements and QUEST questionnaire were collected by researchers not involved in administering the UE-RT and UE-CT.
To reach the objective, all the subjects enrolled were evaluated before the treatment (at baseline) and upon ending the treatment (at week 10) in relation to effectiveness and emotional state outcomes. Feasibility and usability outcomes were evaluated upon ending the treatment.

2.8. Statistical Analysis

The statistical package “Statistical Package for Social Sciences” (version 22; SPSS Inc., Chicago, IL, USA) was used for data analysis. The level of significance was set at 0.05. The Kolmogorov–Smirnov test was applied for verifying normality of baseline data. Therefore, parametric tests were applied to both groups. Results were expressed as mean and standard deviation. At baseline condition, the homogeneity of both groups was proven using the Levene test. The independent t-test was used to compare the score changes between both groups after the treatment. Then, the paired t-test was used to analyze intragroup changes from baseline to ending the treatment. The results of this method were used for calculating the effect size, providing an indication of the magnitude of the differences between the groups analyzed. There are a number of different effect size statistics and one of them is the ɳ2 statistical parameter used in this research. The guidelines proposed by Cohen for interpreting this value are: 0.01, small effect; 0.06, moderate effect; and 0.14, large effect [40,41].
Due to the importance of the dominance in studies related to UE, a sub-analysis was performed considering, for both groups, only the participants who performed the proposed therapy with their dominant arm.

3. Results

Of the 34 subjects enrolled in this study, 3 dropped out of the study before completing the established treatment. One received UE treatment by means of another device (Hand Tutor), the second subject was discharged from the hospital before the end of the treatment, and the third subject’s treatment was interrupted by confinement due to COVID-19 in March 2020. The demographic and functional characteristics of the 31 participants are shown in Table 1, showing the homogeneity of both groups at baseline condition. Therefore, both groups were matched with respect to their cervical metameric level and the severity of injuries suffering the subjects.
Taking into account the dominance aspect, 12 subjects in the control group and 9 subjects in the intervention group received the treatment in the dominant UE.

3.1. Feasibility Outcomes

Statistically significant differences were not found between the two groups analyzed, intervention and control, in relation to the total number of sessions (38.71 (1.89) in the control group (n = 16) versus 37.33 (2.74) in the intervention group (n = 15), p = 0.129), and the weeks spent completing the treatment (9.71 (0.46) in the control group and 9.60 (0.63) in the intervention group, p = 0.587).

3.2. Effectiveness Outcomes between Baseline and Ending Treatment Assessments

Both experimental groups experienced improvements in clinical relevance and statistical significance. However, subjects in the intervention group experienced statistically significant improvement (p1 < 0.05) in the items related to feeding (1.20 (1.14) at baseline versus 1.86 (0.99) upon ending the treatment) and grooming (1.26 (0.96) at baseline versus 1.80 (1.08) upon ending the treatment) (Table 2).
The improvements observed with statistical significance were maintained when the analysis was focused on the dominant UE. In the case of the intervention group (n = 9), the only difference is that no statistical significance was detected in the grooming item (1.55 (1.01) at baseline versus 1.66 (1.22) at the ending, p1 = 0.594). In this case, the magnitude of the difference was small (ɳ2 = 0.037). On the other hand, significance was still detected in the feeding item (1.22 (1.64) at baseline versus 2.00 (1.00) at the ending, p1 < 0.01), which was not detected in the control group (1.16 (1.02) at baseline versus 1.66 (0.98) at the ending, p1 = 0.111, n = 12). However, the magnitude of the improvement in this item was large for the two groups (ɳ2 = 0.494 for the intervention group and ɳ2 = 0.214 for the control group).
The UEMS related to the treated UE was significantly greater upon ending the treatment than at baseline for the control group (15.07 (6.49) versus 13.53 (5.11), p1 = 0.039) and the intervention group (15.60 (5.12) versus 13.13 (5.24), p1 < 0.01) (Figure 4a). In the two groups, the magnitude of the improvement was high, with a large effect (ɳ2 = 0.656 for the intervention group and ɳ2 = 0.255 for the control group) (Table 2). When we focus the analysis on the cases in which the treated arm was the dominant UE, we can observe the loss of statistical significance, maintaining only that which was detected in the intervention group between the assessments at baseline and upon ending the treatment (Figure 4b).
The results related to ROM were expressed as a percentage related to a reference pattern formed by neurologically healthy subjects. No statistically significant differences were found between the assessments at baseline and at the ending in both groups, with the exception of elbow joint range in the control group (106.20 (33.38) versus 148.96 (60.32), p1 < 0.01) (Table 3).
However, with regard to the UE dexterity measured by kinematic indices, significant improvements were observed in both groups. The scores obtained in the smoothness index S1 and in the area of the hexagon describing all of them improved significantly (example in Figure 3). However, the comparison between the baseline and ending conditions for the smoothness S1 index was greater in the intervention group, with greater effect on the observed difference (ɳ2 = 0.438) than in the control group (ɳ2 = 0.281). The improvement in the smoothness S1 was statistically significant in the control group (p1 < 0.05) and in the intervention group (p1 < 0.01) (Table 3, Figure 5a). No statistically significant differences were found in the improvements for the coordination index in the two groups analyzed. However, the magnitude of this improvement was high, with a large effect for the intervention group (ɳ2 = 0.241) (Table 3).
The subjects’ perception of UE use improved progressively in successive assessments using the CUE scale. The graphical results can be seen in Figure 5b, which shows a statistically significant improvement in the subjects in the intervention group (53.28 (18.26) at baseline versus 66.28 (18.20) upon ending the treatment, p1 < 0.01) and those in the control group for this scale (69.18 (8.70) at baseline versus 78.66 (17.04) upon ending the treatment, p1 < 0.01).
With regard to the JTHF test, few subjects were able to perform it at the baseline assessment (seven subjects in the control group and four in the intervention group). However, at the ending assessment, 10 subjects in the control group were able to complete it and 8 patients in the intervention group. This represented an increase of 18.75% in the control group and 26.66% in the intervention group between the two assessments.
Finally, it is of special interest to show, as another outcome measure, the evolution that the subjects experienced in the gravity-compensation levels of the arm and forearm levers of the Armeo Spring. Depending on the progression and evolution of each subject, according to the clinical criteria of the therapist, these levels were modified until reaching a normal situation in terms of gravity (‘E’ for the arm and ‘C’ for the forearm) and even adding resistance, gradually up to a maximum of ‘I’ and ‘E’ in both levers (Figure 6). Only one subject reached these maximum levels during the treatment.

3.3. Changes Inter-Groups after the Treatment

Changes between the groups were made by comparing the differences between measurements at the ending and baseline assessments. Between the baseline and ending assessments, 79.14 (16.30) days elapsed for the control group and 69.50 (12.13) days for the intervention group without statistically significant differences.
In relation to effectiveness outcomes, changes between the groups were analyzed for all the variables registered in the present study (clinical scales and kinematic indices) but statistically significant differences were only observed in the smoothness S1 index measured in the movement pattern executed during the performance of the ADL of drinking from a glass in a real environment. Specifically, the difference observed between the ending and baseline measurements was significantly greater in the intervention group than in the control group (25.51 (19.64) versus 10.75 (17.17), p2 = 0.034) (Table 3). These results are shown in the box plots in Figure 7a. The same results are shown in Figure 7b for when the treated UE is the dominant hand. In this case, the box plot for the intervention group (n = 9) had more amplitude than that for the complete intervention group (n = 15). Moreover, the high improvement observed in one subject of this group appears as a typical value.

3.4. Emotional State Outcomes between Baseline and Ending Treatment Assessments

The results obtained in the two groups analyzed detected a slight disturbance of mood in the BDI at the baseline assessment, which evolved to normal values at the end of the treatment. This improvement was clinically significant (10.17 (6.52) versus 6.58 (5.71), p < 0.05) and the magnitude of the difference was of a large effect size (ɳ2 = 0.269) in the intervention group. As for the HAD Scale, normal values (minor or equal to 7) for depression and anxiety were detected in both assessments without statistically significant differences for the two groups analyzed.

3.5. Usability Outcomes Related to the Armeo Spring Device

In Figure 8, the QUEST questionnaire results are shown, analyzing the three aspects that subjects considered more important, ordered by priority. Thus, the feature of the device that the subjects considered to be the most important was being easy to use, as rated by 9 subjects (60% of the sample comprising the intervention group). This was followed by the comfort of the device, a characteristic rated by 8 subjects (53.33% of the sample), and the third was effectiveness, rated by 10 subjects (66.66% of the sample).
In addition, the subjects forming the intervention group completed another questionnaire using a Likert scale (Table 4). These results will be discussed in the next section and compared with those obtained in a previous study.

4. Discussion

This study has successfully analyzed the effectiveness of the Armeo Spring exoskeleton in improving the performance of subjects with cervical SCI in completing ADL.
Although there are numerous research papers on the Armeo Spring [10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27], very few have focused on analyzing the effectiveness of the device with the idea of detecting findings on the outcomes of UE-RT versus UE-CT. These studies were focused on non-neurological subjects with proximal humeral fracture and surgical treatment [42] and subjects with UE impairments after neurological pathologies such as stroke [43] and cerebral palsy [22]. However, studies carried out on SCI are still scarce compared to these neurological pathologies.
Thus, the only full report on the effectiveness of this device in subacute cervical SCI was published by Zariffa et al., marking a major breakthrough in SCI research. In that study, there was no independent control group that did not receive treatment with the exoskeleton and the authors found few functional benefits in limbs that received Armeo Spring treatment compared to limbs that did not receive treatment with the exoskeleton [13]. For this reason, the experimental protocol in this paper was designed to address some of the shortcomings of this previous study and an independent control group that did not receive exoskeleton therapy was included in the study, thus increasing the sample size.
On the other hand, scientific evidence from one of the most recently published reviews suggests that robotic therapy may not benefit basic ADL more than usual care or no treatment [29]. Therefore, this paper focuses on the possible improvement of robotic therapy in ADL, incorporating within the UL-RT experimental sessions the ADL of drinking, designed for this purpose.

4.1. Feasibility

In accordance with the only previously published report in SCI, our results show that the incorporation of UE-RT into the rehabilitation program of sub-acute SCI inpatients is feasible.
The methodology was designed taking into account the patients’ schedule. The additional treatment time that patients receive was not a limitation to performing the study. Thus, the daily treatment time was increased by 30 min for both groups (30 min of UE-RT for the intervention group and 30 min of UE-CT for the control group), totaling a daily therapy dose of 1 h of duration. Subjects within the control group performed a mean of 38.71 (1.89) experimental sessions during 9.71 (0.46) weeks. These results were similar to those obtained for the intervention group: 37.33 (2.74) sessions during 9.60 (0.63) weeks.

4.2. Effectiveness

In dose-matched trials, there is no evidence that the type of UE-RT is an important factor in the outcome. In the present study, both the control and intervention groups were dose-matched and both of them improved their UE function across the treatment proposed in this methodology. However, this condition, in conjunction with the inclusion of the drinking ADL within the UE-RT sessions, allowed us to detect some differences in the intervention group.
Although both experimental groups improved their level of independence in ADL assessed by means of the SCIM scale, only the intervention group improved their level of independence with statistical significance and clinical relevance in the item related to eating. This may be due to the fact that, within the UE-RT sessions, they worked on the ADL-related gesture of drinking from a glass.
In the JTHF scale, in the intervention group, there was an increase of 26.66% in the subjects who were able to perform the test in the assessment upon ending the treatment compared to the baseline assessment, while in the control group, this increase was of 18.75%.
In relation to the kinematic indices, both experimental groups significantly improved their movement smoothness measured from the peaks number in the hand velocity profile, although the difference between the assessments at the ending and baseline was significantly greater in the intervention group (24.14 (18.48)) than in the control (10.75 (17.17)), probably because the subjects in the intervention group worked with the Armeo Spring on the ADL movement pattern with the appropriate intensity and number of repetitions. In the comparison between groups, it is worth highlighting the result obtained when the analysis was specified to cases in which the treated UE was the dominant one. In this case, no statistical significance was obtained between the groups. However, in the intervention group, an increase in the amplitude of the box plot was observed and the case of the subject who experienced the greatest improvement in smoothness of movement did not appear as an outlier or atypical result within the sample analyzed, thus reflecting the importance of taking dominance into account in these studies.
On the other hand, although the improvement observed in the coordination index was not statistically significant, it was considered clinically relevant in the intervention group due to the calculated effect size. In view of the results, it appears that UE-RT and the virtual reality application for the drinking task have a positive influence on the movement pattern of the UE during the performance of the ADL of drinking in a real environment, as determined through the intensity, number of repetitions, motivation, sources of feedback provided by robotic therapy, and the novel virtual environment used by the Armeo Spring device.
The inclusion of the kinematic indices as an assessment method is a strength of the present study and complements a previous study published by us with a minor sample size [44]. In this previous study, all the participants were evaluated only by means of the Capabilities of Upper Extremity (CUE) Questionnaire and the SCIM scale with the aim of analyzing the impact of robotic therapy in the self-perception of limited UE function that SCI patients have and analyzing the correlation between both clinical scales. This correlation was higher at the ending of the study than at baseline for both groups, obtaining a correspondence between patients’ self-perception and their functional independence. In addition, the present study was complemented with anxiety and depression evaluations, obtaining that the results in the present study were not influenced by the emotional state of the subjects participating in this study, since findings of anxiety and depression were not detected by the BDI and HAD scales.
Another measurement of effectiveness to consider in the case of the UE-RT by means of the Armeo Spring is the evolution of the subjects in the gravity-compensation parameters of the arm and forearm levers of the exoskeleton.

4.3. Usability Questionnaires

The three aspects of the device that the subjects rated as most important were ease of use, comfort, and effectiveness, determined by the Likert scale for the subjects to provide feedback about their experience with the Armeo Spring device. Although, in our study, the scores on the questions asked were slightly higher than in the previous study by Zariffa et al. [13], the subjects’ opinion was quite similar. Subjects found the exoskeleton Armeo Spring easy to use and useful for recording progress during treatment. In addition, they found the number and duration of sessions to be adequate. With regard to the two additional questions concerning the drinking ADL, subjects considered that the virtual reality application of the drinking ADL enriched the therapy proposed with the Armeo Spring and that it was useful for working on this ADL. However, despite these benefits, subjects did not express any preference for using UE-RT over UE-CT. They always considered the robotic therapy as complementary to the conventional therapy they usually received. Of particular interest is when we asked subjects if they considered the device appropriate for someone with the same level of injury and severity. Subjects with very low cervical SCI and who were incomplete in the motor aspects told us that they felt it was appropriate but that fine hand dexterity was not something they could work on with the Armeo Spring. This helped us to address future research towards finding a technological solution primarily focused on hand treatment.

4.4. Study Limitations

Some limitations have been identified in this study. The subjects were usually discharged very close to the end date of the experimental study. Therefore, although the subjects were able to complete the study in terms of the proposed number of experimental sessions and duration of treatment, the main limitation is the lack of a follow-up assessment for analyzing if the improvements observed in subjects were retained over time. Thus, the next reasonable step would be to increase this sample size in the context of a funded study in which a follow-up assessment is planned for all the subjects.
Another limitation is the ceiling effect that the Armeo Spring has, found for one subject with a cervical SCI of metameric level C8 and ASIA C classification, making it clear that there is a need to find an additional technology for specific hand treatment with the aim of complementing the therapy that the subjects received with the Armeo Spring. This has led us to search for other hand-focused technologies to complement the therapies administered in this study. An example of this is the Leap Motion Controller, for which a set of virtual applications with a therapeutic meaning have been developed in our center [45].
A strength of this study is worth mentioning. This study has been achieved with the coordinated collaboration of three different clinical units or departments of the hospital, with the contributions of physicians, occupational therapists, engineers, and a neuropsychologist. In addition, the experimental groups were dose-matched and it has been proven that the robotic therapy improves the level of independence in ADL in this population.
Finally, it is interesting to think about the proposal of possible improvements to the methodology followed in the present study. One of them could be to more comprehensively control the amount of conventional therapy related to ADL that the patients receive. And, probably, one should be to propose a pairwise analysis comparing a patient in the intervention group with the most similar patient in the control group in terms of the level and severity of their lesion and functional characteristics.

5. Conclusions

Assistive technologies are achieving a very important role in the rehabilitation of neurological patients. They promote improvements in motor function in those tasks trained by means of robotic therapy. They undoubtedly serve to administer physical therapy, complementing the conventional therapies that patients receive.
The results obtained in the present study supported the preliminary findings found in the previous study published by us [44], and the influence of robotic therapy (Armeo Spring in this case) over patients’ improvement in ADL has been demonstrated with a higher punctuation in the SCIM scale in terms of self-care items and the smoothness kinematic index measured during the performance of the ADL of drinking from a glass in a real environment. This ADL was the same that patients trained by means of the Armeo Spring device.
In conclusion, as future research, it would be of interest to incorporate the computation of kinematic indices from the kinematic data collected during the performance of the drinking ADL with the Armeo Spring to check whether the subjects with cervical SCI are performing the movement pattern similar to the healthy pattern from a neurological point of view. It is necessary to take into account that these kinematic indices would be computed from the kinematic data obtained through a postural estimator of the UE implemented within the software of the Armeo Spring, by means of the collaboration maintained with Vicomtech [46]. This would be another important engineering contribution to the clinical environment. Finally, to increase this sample in the context of a funded study in which a follow-up assessment is planned for all the subjects would be interesting.

Author Contributions

Conceptualization, M.A.-M., A.G.-A., A.d.l.R.-G. and A.G.-A.; methodology, V.L.-B.; M.A.-M., R.P.-G. and Y.P.-B.; software, A.d.l.R.-G. and C.C.; validation, M.A.-M., A.G.-A. and A.d.l.R.-G.; formal analysis, V.L.-B., B.P.-L. and A.d.l.R.-G.; investigation, V.L.-B., R.P.-G., Y.P.-B., B.P.-L. and A.d.l.R.-G.; resources, M.A.-M., A.G.-A., C.C. and A.d.l.R.-G.; data curation, V.L.-B., R.P.-G., Y.P.-B. and A.d.l.R.-G.; writing—original draft preparation, V.L.-B., M.A.-M., R.P.-G., Y.P.-B., B.P.-L., A.G.-A., C.C. and A.d.l.R.-G.; writing—review and editing, V.L.-B., M.A.-M., R.P.-G., Y.P.-B., B.P.-L., A.G.-A., C.C. and A.d.l.R.-G.; supervision, M.A.-M., A.G.-A., B.P.-L., C.C. and A.d.l.R.-G.; project administration, A.G.-A. and A.d.l.R.-G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee of Comité Ético de Investigación Clínica, Complejo Hospitalario de Toledo (Approval number: 85, date of approval: 14/06/2016).

Informed Consent Statement

Written informed consent has been obtained from all the patients involved in the study.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

We acknowledge all participants (hospital staff and patients) who accepted voluntarily to be part of this study.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. CONSORT flow chart.
Figure 1. CONSORT flow chart.
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Figure 2. Subject instrumented with Armeo Spring device during a robotic therapy upper extremity session.
Figure 2. Subject instrumented with Armeo Spring device during a robotic therapy upper extremity session.
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Figure 3. Graphical results related to the kinematic assessments for one participant.
Figure 3. Graphical results related to the kinematic assessments for one participant.
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Figure 4. (a) Upper extremity motor score (UEMS) of the upper limb treated for both groups when the total sample is analyzed (control group (n = 16) and intervention group (n = 15)); (b) upper extremity motor score (UEMS) of the upper limb treated for both groups when the treated arm was the dominant arm (control group (n = 12) and intervention group (n = 9)). Dark grey represented the control group. * p < 0.05, ** p < 0.01.
Figure 4. (a) Upper extremity motor score (UEMS) of the upper limb treated for both groups when the total sample is analyzed (control group (n = 16) and intervention group (n = 15)); (b) upper extremity motor score (UEMS) of the upper limb treated for both groups when the treated arm was the dominant arm (control group (n = 12) and intervention group (n = 9)). Dark grey represented the control group. * p < 0.05, ** p < 0.01.
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Figure 5. (a) Graphical results in relation to the smoothness kinematic index for both groups analyzed (dark grey represents the control group). The asterisks show the statistical significance (* (p < 0.05) and ** (p < 0.01)); (b) graphical results in relation to the Capabilities of Upper Extremity (CUE) Questionnaire clinical scale for both groups analyzed. The asterisks show the statistical significance (* (p < 0.05) and ** (p < 0.01)).
Figure 5. (a) Graphical results in relation to the smoothness kinematic index for both groups analyzed (dark grey represents the control group). The asterisks show the statistical significance (* (p < 0.05) and ** (p < 0.01)); (b) graphical results in relation to the Capabilities of Upper Extremity (CUE) Questionnaire clinical scale for both groups analyzed. The asterisks show the statistical significance (* (p < 0.05) and ** (p < 0.01)).
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Figure 6. Subjects’ evolution in the configurable parameters of Armeo Spring, such as the gravity-compensation levels: (a) for the arm lever; (b) for the forearm lever.
Figure 6. Subjects’ evolution in the configurable parameters of Armeo Spring, such as the gravity-compensation levels: (a) for the arm lever; (b) for the forearm lever.
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Figure 7. Inter-group comparison for the smoothness kinematic index for both groups: (a) when the total sample is analyzed; (b) when the treated arm was the dominant arm. The asterisks show the statistical significance (* p < 0.05).
Figure 7. Inter-group comparison for the smoothness kinematic index for both groups: (a) when the total sample is analyzed; (b) when the treated arm was the dominant arm. The asterisks show the statistical significance (* p < 0.05).
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Figure 8. Subject instrumented with Armeo Spring device during a robotic therapy upper extremity session. Results related to QUEBEC User’s Evaluation of Satisfaction with Assistive Technology (QUEST) for the three aspects of the device that subjects within the intervention group consider more important by priority order.
Figure 8. Subject instrumented with Armeo Spring device during a robotic therapy upper extremity session. Results related to QUEBEC User’s Evaluation of Satisfaction with Assistive Technology (QUEST) for the three aspects of the device that subjects within the intervention group consider more important by priority order.
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Table 1. Demographic characteristics of the sample analyzed.
Table 1. Demographic characteristics of the sample analyzed.
VariablesSample Analyzed
Control Group (n = 16)Intervention Group (n = 15)Levene Test
Gender (Male) *11.00 (68.75)10.00 (66.67)F = 0.057, p = 0.813
Age (years) +42.44 (15.82)37.73 (16.08)F = 0.043, p = 0.837
Injury level *
C2-1.00 (6.66)
C31.00 (6.25)1.00 (6.66)
C46.00 (37.50)4.00 (26.68)F = 0.029, p = 0.867
C5 6.00 (37.50)7.00 (46.68)
C61.00 (6.25)1.00 (6.66)
C72.00 (12.50)1.00 (6.66)
AIS classification *
A4.00 (25.00)4.00 (26.68)
B3.00 (18.75)3.00 (19.98)F = 0.135, p = 0.716
C2.00 (12.50)1.00 (6.66)
D 7.00 (43.75)7.00 (46.68)
Time since injury (months) +4.11 (1.31)4.12 (1.67)F = 2.925, p = 0.098
Treated arm (right) *12.00 (75.00)10.00 (66.67)F = 0.966, p = 0.334
Dominant arm (right) *13.00 (81.25)14.00 (93.33)F = 1.185, p = 0.285
UEMS (0–25) + (treated arm)13.81 (5.06)13.13 (5.24)F = 0.016, p = 0.899
+ continuous variables are expressed as mean and standard deviation; * categorical variables are expressed as frequency and percentage.
Table 2. SCIM scale and UEMS at baseline and upon ending all the experimental sessions for both groups included in the study (control and intervention).
Table 2. SCIM scale and UEMS at baseline and upon ending all the experimental sessions for both groups included in the study (control and intervention).
Control Group (n = 16)Intervention Group (n = 15)p2
At BaselineAt EndingDifference At BaselineAt EndingDifference
Mean (SD)Mean (SD)Mean (SD)p1Ƞ2Mean (SD)Mean (SD)Mean (SD)p1Ƞ2
SCIM scale
Feeding1.31 (1.07)1.75 (0.85)0.43 (1.03)0.1100.161 **1.20 (1.14)1.86 (0.99)0.73 (0.96)0.0270.303 **0.416
Dressing Upper Body0.56 (1.09)1.68 (0.87)1.12 (1.45)0.0070.389 **0.80 (1.37)1.53 (1.76)0.73 (1.22)0.0360.278 **0.425
Grooming1.43 (1.20)1.87 (1.08)0.43 (1.26)0.1860.113 *1.26 (0.96)1.80 (1.08)0.60 (0.82)0.0410.266 **0.677
Self care Subtotal (0–20)4.06 (4.38)8.06 (6.15)3.93 (4.90)0.0050.416 **3.53 (3.58)7.46 (6.61)4.06 (4.97)0.0100.391 **0.943
Total SCIM Score (0–100)31.00 (18.52)45.87 (23.79)14.25 (12.36)0.0000.614 **30.06 (16.86)44.26 (23.95)14.40 (15.55)0.0030.469 **0.976
UEMS (Arm treated) (0–25)13.53 (5.11)15.07 (6.49)0.31 (5.49)0.0390.255 **13.13 (5.24)15.60 (5.12)2.46 (1.84)0.0000.656 **0.160
* moderate effect and ** large effect (clinical relevance following Cohen guidelines). Bold font indicates significant statistical differences found between baseline and ending assessments for both groups (control and intervention). p1: intragroup comparison (comparison of baseline and ending scores with paired sample t-test), p2: inter-group comparison (comparisons of differences of baseline-ending scores with the independent t-test). Bold p1 and p2 values are statistically significant (p < 0.05).
Table 3. Effectiveness variables in terms of range of motion and kinematic indices at baseline and upon ending all the experimental sessions for both groups included in the study (control and intervention).
Table 3. Effectiveness variables in terms of range of motion and kinematic indices at baseline and upon ending all the experimental sessions for both groups included in the study (control and intervention).
Control Group (n = 16)Intervention Group (n = 15)p2
At BaselineAt EndingDifference At BaselineAt EndingDifference
Mean (SD)Mean (SD)Mean (SD)p1Ƞ2Mean (SD)Mean (SD)Mean (SD)p1Ƞ2
Range of motion (%)
Shoulder67.10 (28.56)57.74 (17.73)−9.35 (23.17)0.1400.158 **70.25 (23.12)63.75 (22.56)−6.50 (28.00)0.3840.0580.763
Elbow106.20 (33.38)148.96 (60.32)37.01 (99.02)0.0080.477 **122.38 (51.51)119.91 (50.77)6.16 (70.38)0.8880.0010.346
Wrist264.70 (154.19)192.24 (85.01)−72.45 (160.62)0.1460.196 **268.56 (133.19)235.64 (106.63)−6.91 (172.22)0.4110.0560.321
Total98.83 (31.95)107.16 (38.40)15.28 (37.78)0.3040.104 *107.81 (35.96)100.51 (22.28)2.44 (53.56)0.5010.0380.477
Kinematic Indices (%)
Efficiency66.92 (35.21)86.90 (32.96)19.98 (38.58)0.0560.234 **89.51 (57.49)86.91 (28.86)−2.59 (55.89)0.8600.0020.198
Accuracy46.36 (29.56)52.21 (23.55)5.84 (27.17)0.4030.04650.09 (29.30)52.74 (26.81)2.64 (26.03)0.7000.0100.741
Agility43.13 (31.00)50.31 (23.27)7.17 (25.58)0.2800.077*46.06 (30.07)50.78 (27.67)4.72 (24.16)0.4620.0390.786
Smoothness (S1)44.86 (17.96)57.48 (24.73)10.75 (17.17)0.0280.281 **45.18 (31.49)62.69 (46.41)25.51 (19.64)0.0050.438 **0.034
Smoothness (S2)64.27 (19.47)86.00 (29.16)21.73 (35.43)0.0270.286 **78.31 (21.61)92.50 (22.52)14.18 (25.98)0.0530.241 **0.506
Coordination92.84 (19.16)93.83 (18.10)0.99 (18.06)0.8290.00378.18 (17.27)90.35 (20.65)12.16 (26.14)0.0930.188 **0.175
Area36.40 (19.95)51.43 (24.13)15.03 (19.86)0.0080.379 **43.10 (26.21)56.35 (33.67)13.24 (13.86)0.0020.494 **0.775
Reaching amplitude71.26 (23.72)74.66 (16.95)3.39 (20.21)0.5110.03179.85 (27.43)76.96 (15.89)−2.89 (15.84)0.4910.0340.345
* Moderate effect and ** large effect (clinical relevance following Cohen guidelines). Bold font indicates statistically significant differences found between baseline and ending assessments for both groups (control and intervention). p1: intragroup comparison (comparison of baseline and ending scores with paired sample t-test), p2: inter-group comparison (comparisons of differences baseline-ending scores with the independent t-test). Bold p1 and p2 values are statistically significant (p < 0.05).
Table 4. Results related to the subject discharge questionnaire for patients within the intervention group. Results are shown with mean score and standard deviation for each question.
Table 4. Results related to the subject discharge questionnaire for patients within the intervention group. Results are shown with mean score and standard deviation for each question.
QuestionMean (SD)
Q1. The ARMEO was enjoyable to use.6.4 (0.8)
Q2. It was easy to understand how to use the ARMEO.6.8 (0.4)
Q3. The games increased your motivation to perform your exercises.6.0 (1.2)
Q4. You would be comfortable using the ARMEO with only minimal supervision by a therapist.4.6 (1.9)
Q5. You felt that the ARMEO training was an effective for rehabilitation as your usual rehabilitation sessions with a therapist.5.3 (1.2)
Q6. The ARMEO was helpful for tracking the progress of your rehabilitation.6.4 (0.9)
Q7. The length of the sessions was appropriate6.8 (0.4)
Q8. The number of sessions per week was appropriate6.7 (0.4)
Q9. You felt that the ARMEO exercises were more relevant to activities in your daily life than conventional rehabilitation.4.3 (1.0)
Q10. You think that the ADL drinking game enriches the therapy proposed by ARMEO6.7 (0.6)
Q11. You find this game useful for ADL training6.6 (0.7)
Q12. You would use the ARMEO in your free time if it was available to you.5.8 (1.6)
Q13. You preferred the ARMEO training to conventional rehabilitation. 4.3 (1.5)
Q14. The ARMEO is appropriate for someone with your level of lesion.6.7 (0.8)
Q15. The ARMEO is appropriate for someone with your type of injury (that is, AIS A, B, C or D)6.4 (1.2)
AIS, ASIA Impairment Scale.
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MDPI and ACS Style

Lozano-Berrio, V.; Alcobendas-Maestro, M.; Perales-Gómez, R.; Pérez-Borrego, Y.; Gil-Agudo, A.; Polonio-López, B.; Cortés, C.; de los Reyes-Guzmán, A. Can Robotic Therapy Improve Performance in Activities of Daily Living? A Randomized Controlled Trial in Sub-Acute Spinal Cord Injured Patients. Appl. Sci. 2024, 14, 8478. https://doi.org/10.3390/app14188478

AMA Style

Lozano-Berrio V, Alcobendas-Maestro M, Perales-Gómez R, Pérez-Borrego Y, Gil-Agudo A, Polonio-López B, Cortés C, de los Reyes-Guzmán A. Can Robotic Therapy Improve Performance in Activities of Daily Living? A Randomized Controlled Trial in Sub-Acute Spinal Cord Injured Patients. Applied Sciences. 2024; 14(18):8478. https://doi.org/10.3390/app14188478

Chicago/Turabian Style

Lozano-Berrio, Vicente, Mónica Alcobendas-Maestro, Raquel Perales-Gómez, Yolanda Pérez-Borrego, Angel Gil-Agudo, Begoña Polonio-López, Camilo Cortés, and Ana de los Reyes-Guzmán. 2024. "Can Robotic Therapy Improve Performance in Activities of Daily Living? A Randomized Controlled Trial in Sub-Acute Spinal Cord Injured Patients" Applied Sciences 14, no. 18: 8478. https://doi.org/10.3390/app14188478

APA Style

Lozano-Berrio, V., Alcobendas-Maestro, M., Perales-Gómez, R., Pérez-Borrego, Y., Gil-Agudo, A., Polonio-López, B., Cortés, C., & de los Reyes-Guzmán, A. (2024). Can Robotic Therapy Improve Performance in Activities of Daily Living? A Randomized Controlled Trial in Sub-Acute Spinal Cord Injured Patients. Applied Sciences, 14(18), 8478. https://doi.org/10.3390/app14188478

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