Journal Pre-proof

Robotic-assisted gait training (RAGT) in stroke rehabilitation: a pilot

study

Mariana Vita Milazzotto Neves MSc , Leonardo Furlan PhD ,

Felipe Fregni MD, PhD , Linamara Rizzo Battistella MD, PhD ,
Marcel Simis MD, PhD

PII: S2590-1095(23)00002-2
DOI: https://doi.org/10.1016/j.arrct.2023.100255
Reference: ARRCT 100255

To appear in: Archives of Rehabilitation Research and Clinical Translation

Please cite this article as: Mariana Vita Milazzotto Neves MSc , Leonardo Furlan PhD ,
Felipe Fregni MD, PhD , Linamara Rizzo Battistella MD, PhD , Marcel Simis MD, PhD , Robotic-
assisted gait training (RAGT) in stroke rehabilitation: a pilot study, Archives of Rehabilitation Research
and Clinical Translation (2023), doi: https://doi.org/10.1016/j.arrct.2023.100255

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This is an open access article under the CC BY-NC-ND license
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Robotic-assisted gait training (RAGT) in stroke rehabilitation: a pilot study

Mariana Vita Milazzotto Neves, MSc1 , Leonardo Furlan, PhD1 , Felipe Fregni, MD,
PhD2 , Linamara Rizzo Battistella, MD, PhD1 , Marcel Simis, MD, PhD1

1. Physical and Rehabilitation Medicine Institute, General Hospital, Medical

School of the University of Sao Paulo, Sao Paulo, Brazil

2. Neuromodulation Center and Center for Clinical Research Learning,

Spaulding Rehabilitation Hospital and Massachusetts General Hospital,
Harvard Medical School, Boston, Massachusetts, USA

Ethics approval and consent to participate

The present research has been approved by the Ethics Committee for Analysis of
Research Projects (CAPPesq) from the University of São Paulo’s Faculty of Medicine
and written consent was obtained from each participant (Plataforma Brasil
15138519.0000.0068).

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the
corresponding author on reasonable request.

Competing interests
The authors declare that they have no competing interests.

Funding
This work was supported by Núcleo de Apoio a Pesquisa – Núcleo de Estudos
Avançados em Reabilitação (NAP – NEAR). The researchers received support from the
São Paulo Research Foundation (FAPESP – SPEC, grant #2017/12943-8).

Authors' contributions
MVMN collected the data. MS analysed and interpreted the data. MVMN wrote the first
draft of the manuscript. LF extensively revised the first draft of the manuscript. FF,
LRB and MS revised and approved all subsequent versions of the manuscript. All
authors read and approved the final version of the manuscript.

Acknowledgements
The authors are grateful to Margarida H. Miyazaki (executive director of IMREA),
Mariane Tateishi, Katia Lina Miyahara (Clinical Director of IMREA), Artur César
Aquino dos Santos, Maria Cecília dos S. Moreira and Denise V. M. Ayres (Directors of
Physiotherapy Service) and the physiotherapy group from IMREA.

Corresponding author
Marcel Simis (marcel.simis@hc.fm.usp.br), Rua Domingo de Soto, 100 - Jardim Vila
Mariana, São Paulo - SP, 04101-300, +55 (11) 51807800.

1
Robotic-assisted gait training (RAGT) in stroke rehabilitation: a pilot study

Abstract

Objective: To compare the effects of two types of robotic-assisted gait training (RAGT)

devices that have been used in stroke rehabilitation.

Design: Retrospective cohort.

Setting: Rehabilitation hospital.

Participants: 24 community dwelling people with stroke.

Interventions: RAGT with either an exoskeleton (Lokomat) (mean age = 53.8; 30%

male; mean duration of stroke = 17.8 months) or an end-effector (G-EO) (mean age =

50.5; 77.8% male; mean duration of stroke = 13.11) delivered 3 times per week (36

sessions total).

Main Outcome Measures: The following tests/scales were employed before and after

RAGT: Functional Ambulation Categories (FAC), Timed Up and Go (TUG), 10-Metre

Walk Test (10MWT), 6-Minute Walk Test (6MWT), Trunk Impairment Scale (TIS),

Dynamic Gait Index (DGI), Berg Balance Scale (BBS) and ability to climb stairs (time

to climb six steps of 15cm each; ACS).

Results: There were 5 dropouts, all from the G-EO group. At the end, 10 participants in

the Lokomat and 9 in the G-EO group completed the intervention. From pre- to post-

RAGT, G-EO patients improved on all functional tests/scales, whereas Lokomat

patients improved only on the TUG, DGI and BBS. Most patients showed

improvements above the relative smallest real difference (SRD%) in the TUG, 10MWT

and 6MWT.

Conclusions: Both end-effectors and exoskeletons may improve clinically relevant

aspects of walking function. However, this study had a small sample, was retrospective,

2
non-randomized, and had a significant number of drop-outs, therefore its findings

should be interpreted carefully. Future studies are needed for investigating potential

differences in clinical results, side effects, contraindications and cost effectiveness

between these two different types of RAGT.

Key Words: Stroke; Rehabilitation; Exoskeleton Device; Robotics.

List of Abbreviations

RAGT – Robotic-Assisted Gait Training

FAC – Functional Ambulation Category

TUG – Timed Up and Go

10MWT – Ten Meter Walk Test

6MWT – Six Minute Walk Test

TIS – Trunk Impairment Scale

DGI – Dynamic Gait Index

BBS – Berg Balance Scale

ACS – Ability to Climb Stairs

SRD% - Smallest Real Difference

1. Background

Stroke is a major cause of death and disability worldwide (1). After stroke, many

patients are left with gait impairments which restrict their physical independence and

participation in activities of daily living and thereby contribute to a reduced quality of

life. For instance, the literature suggests that approximately 20-40% of patients remain

dependent or have no walking function six months after a stroke (2). Therefore,

3
developing effective rehabilitation strategies to restore or improve walking after stroke

is of paramount importance.

Current clinical practice guidelines recommend that people with stroke perform

task-specific walking training at moderate to high aerobic intensities in order to improve

walking function, in terms of either walking speed or distance (3). In daily clinical

practice, however, offering patients the opportunity to practice walking at such aerobic

intensities is rather challenging, for both the patients themselves and the therapists, who

often need to provide manual support and guidance. Another challenge is to give any

opportunity at all of task-specific training to patients with very limited mobility and

balance, who cannot stand and/or walk independently. One way to overcome these

challenges is through automated or robotic-assisted gait training (RAGT) (4).

Two types of RAGT device have been most frequently employed in walking

rehabilitation research after stroke, namely, exoskeletons and end-effectors.

Exoskeletons consist of a body weight support system, a treadmill and an exoskeleton

that moves the patients’ lower limbs over the treadmill according to pre-programed gait

patterns. End-effectors, on the other hand, are composed of a body weight support

system and two footplates that move the patients’ feet simulating gait patterns (4).

A recent Cochrane meta-analysis (5) showed that people with stroke who

receive RAGT in addition to physiotherapy are 2 times more likely to achieve walking

independence than patients receiving only physiotherapy or usual care (OR 2.01, 95%

CI [1.51-2.69]). Moreover, RAGT was shown to be safe and acceptable among patients.

This evidence was of high-quality, consolidating the benefits of RAGT (5).

The authors of that review also found that the type of RAGT device used

(exoskeleton vs end-effector) had no effect in terms of achieving independent walking,

but that end-effectors may be better suited for achieving higher walking speeds (in

4
meters per second) and capacities (meters walked in 6 minutes) (5). This finding

corroborates the results of a previous network meta-analysis, which showed that end-

effectors, but not exoskeletons improve both walking speed and distance (6). However,

the specific benefits of each of these devices need to be better understood (5).

Determining whether exoskeletons and end-effectors are superior to one another has

important implications for clinical practice since their costs are substantially different.

We performed a retrospective analysis of a cohort of people with stroke who

received RAGT in our institution, with either an exoskeleton or an end-effector device,

in addition to conventional physiotherapy. Our aim was to describe the performance of

the two RAGT devices in terms of their ability to improve walking as well as to

investigate the potential mechanisms underlying any performance differences between

them.

2. Methods

The present research consists of a secondary analysis of the data pertaining to a

prospective cohort study of people with stroke undergoing rehabilitation in our

institution (NCT02432521). The present research has been approved by the Ethics

Committee for Analysis of Research Projects (CAPPesq) from the University of São

Paulo’s Faculty of Medicine and written consent was obtained from each participant.

The use of the data for this ancillary study was properly approved by the ethics

committee and provided for in the consent form. Patients were recruited from the stroke

rehabilitation service of the Lucy Montoro hospital, Physical Medicine and

Rehabilitation Institute, Clinics Hospital, Faculty of Medicine, University of São Paulo.

2.1. Eligibility Criteria

5
The inclusion criteria were: age over 18 years, clinical and neuroimaging-based

diagnosis of stroke, more than 1 month since the stroke and clinical stability. The

exclusion criteria were: musculoskeletal pain or deformities that could interfere with the

execution of the therapy, psycho-affective disorders that could influence adherence to

treatment, being a participant in another lower limb rehabilitation study, destabilization

of clinical comorbidities, and contraindications to RAGT.

2.2. Allocation Criteria

Patients were evaluated by a physiatrist who prescribed RAGT without specifying the

type of device (exoskeleton or end-effector). The allocation was not randomized and

was mainly based on the scheduling availability of the RAGT device and therefore was

not influenced by the researchers, therapists nor the physician.

2.3. Patient Stratification

Patients were classified as either moderately or mildly impaired in terms of walking

function according to their Functional Ambulation Categories (FAC) test’s score.

Patients with a score of 2 or 3 were classified as moderate while patients scoring 4 or 5

were considered mild (see below). Because patients who are more severely impaired

(e.g., FAC score < 2) cannot be promptly treated with end-effector devices, they were

not included in this study.

2.4. Intervention

The RAGT devices used were the G-EOa (end-effector) and the Lokomat b (exoskeleton).

The intervention was delivered 3 times per week in a total of 36 sessions. A team of

trained and certified clinicians was responsible for the training with the two devices.

6
 For the G-EO device, the protocol consisted of 20 minutes of training. Patients

practiced gait and stair climbing (up and down). The first 5 minutes of the protocol

consisted of a warm-up phase, during which patients were instructed to walk at a pre-

determined speed according to their walking test’s result. For the Lokomat device, the

protocol consisted of 30 minutes of gait training. All sessions were supervised by a

trained physiotherapist. Vital signs were monitored before, during and after training

with both devices, and gait speed and weight bearing were adjusted at the individual

level according to tolerance and progress.

During their period of RAGT, all patients took part in the conventional stroke

rehabilitation program of our institution, which consisted of global stretching and

strengthening exercises, balance and overground gait training. No body weight

supported treadmill training was allowed during this period.

2.5. Assessments

Patients were assessed for their functional status before and after the 36 sessions of

RAGT. Demographic data and history were obtained at the initial assessment and from

the patients’ records. The following functional tests/scales were used: Functional

Ambulation Categories (FAC), Timed Up and Go (TUG), 10-Metre Walk Test

(10MWT), 6-Minute Walk Test (6MWT), Trunk Impairment Scale (TIS), Dynamic Gait

Index (DGI), Berg Balance Scale (BBS) and ability to climb stairs (ACS; time to climb

six steps of 15cm each). These tests/scales are widely employed in post-stroke walking

rehabilitation research. The assessments were performed by trained physiotherapists

who were not blind for the type of RAGT device.

2.6. Statistical Analysis

7
Statistical analysis was performed with STATAc. Due to our small sample, non-

parametric tests were used. To test for within-group changes, the Wilcoxon signed rank

test was used. The level of significance was set at p < 0.05 (two-sided). Patients who

could not perform the assessments at baseline were excluded from these analyses.

Moreover, we calculated the proportions of patients showing real improvements

in TUG, 10MWT and 6MWT from pre- to post-RAGT. “Real improvements” means

improvements that exceed random measurement error and therefore reflect true

modifications in physical performance/function. For determining whether

improvements were real, we used relative smallest real difference (SRD%) threshold

values that have been published for TUG, 10MWT and 6MWT (7). Relative

improvements ([change score/baseline score] x 100) equal to or higher than 23, 22 and

13% were considered real improvements in TUG, 10MWT and 6MWT, respectively

(7). Patients who could perform these tests after, but not before treatment, were also

considered as showing real improvements.

3. Results

Twenty-four patients took part in the present study. Five patients from the G-EO group

did not complete the 36 sessions of training. Two of these patients were discharged due

to social reasons unrelated to their rehabilitation or participation in the study, two

because of knee pain and one due to an arm fracture at home. Of the remaining patients

who completed the study, most were mildly impaired, 10 received RAGT with Lokomat

and 9 with G-EO (Table 1).

The number of patients who could not perform the functional assessments at

baseline were four for DGI (two G-EO and two Lokomat), one for BBS (G-EO), one for

TIS (Lokomat), two for TUG (one G-EO and one Lokomat), two for 10MWT (one G-

8
EO and one Lokomat), three for 6MWT (one G-EO and two Lokomat) and four for ACS

(two G-EO and two Lokomat). Two patients from the G-EO group who were not able to

perform the assessments before treatment became able to perform it after RAGT; one

became able to perform the TUG test and the other the ACS test.

Patients from the G-EO group showed statistically significant improvements

from baseline to post-training on all functional tests/scales employed (Table 2),

whereas in the Lokomat group, patients improved only on TUG, DGI and BBS (Table

3).

The percentages of patients who achieved “real improvements” are described in

Table 4.

4. Discussion

We analyzed the data from people with stroke who underwent walking rehabilitation in

our institution in order to compare the exoskeleton (Lokomat) and end-effector (G-EO)

types of RAGT devices, in terms of their ability to improve walking function. From

baseline to post-training, G-EO patients improved on all functional tests/scales

employed, whereas Lokomat patients improved only on TUG, DGI and BBS. This

seeming difference between the two systems might be the result of an inflated type I

error rate due to uncorrected multiple testing, leading to false-positive findings in the G-

EO group. However, it is also possible that differences in the training provided by each

system induced distinct effects.

For instance, the RAGT provided by the end-effector might have facilitated the

standing up movement of the TUG test through better control and/or strengthening of

the hip and knee extensor muscles. For example, walking training with end-effectors

might impose greater knee extension demands than with exoskeletons (8). Moreover, the

9
stair climbing training provided by the G-EO device might have contributed to increase

hip and knee extension control and/or strength to a greater extent. However, these

hypotheses need to be empirically confirmed in the future.

With regards to the ACS test, patients in the G-EO group had a moderate effect-

size (0.63) whereas those in the Lokomat had a small effect-size (0.10). The G-EO

device essentially trains movements that are similar to the ones applied in the ACS test,

which is an adapted test used in our institution to measure the time in seconds that

patients take to climb 6 steps of 15cm each. This feature of the training could have

facilitated the transfer of training effects, hence leading to greater improvements in the

ACS test. This argument is theoretically supported by the principle of the ‘specificity of

training effects’, which states that the effects of training are specific to the muscles,

movements or tasks that were trained (9). Further support to this hypothesis comes from

the empirical observation of Hesse and colleagues, who found comparable activation

patterns for the quadriceps muscle of people with stroke during real and end-effector-

simulated stair climbing (8).

The finding that G-EO but not Lokomat patients showed statistically significant

improvements in walking speed and capacity, as assessed through the 10MWT and

6MWT, respectively, is in keeping with the results from previous meta-analyses (5,6).

A recent small observational study also reported no significant changes in walking

speed after training with a wearable/mobile powered exoskeleton (10). The reasons for

this apparent difference have not yet been clarified and there is great heterogeneity

among studies (5), so further research addressing this issue is currently needed. It is

possible that peculiarities of the training regime with end-effectors are driving these

differences between the two types of RAGT device. For instance, as suggested by our

results, end-effector training might induce greater improvements in hip, knee, and trunk

10
strength and control, as well as in overall balance, as revealed by the results from the

TUG, TIS, BBS, and ACS tests/scales. Moreover, it is also possible that a higher

proportion of males and of patients at a lower chronicity level in the G-EO group have

played a role as well.

The proportion of patients showing real improvements from pre- to post-RAGT

was similar between the G-EO and Lokomat groups. The finding that some patients did

not show real improvements after RAGT may be related to the fact that most of our

sample was in the chronic phase of stroke (> 6 months). Besides, all patients had had

their stroke for more than 3 months, which is considered the period of greatest plasticity

and recovery (11). On the other hand, the fact that most patients from both groups

together showed real improvements (Table 4) demonstrates that meaningful gains are

still possible in the chronic phase of stroke through intensive task-specific training and

corroborates the findings from other studies (12).

The observation that both groups improved on the DGI and BBS from baseline

to post-training suggests that either end-effectors or exoskeletons may be used after

stroke for balance training, which is a critical component of any comprehensive walking

rehabilitation program. It is likely that the lack of improvement in the TIS that was

observed in the Lokomat, but not in the G-EO group, was due to the lower trunk control

demand imposed by the exoskeleton device.

Overall, our results show that both end-effectors and exoskeletons improve

clinically relevant aspects of walking function, as assessed through the tests/scales

TUG, DGI, BBS and ACS. Moreover, it seems that for at least some walking-related

functions end-effectors might be superior to exoskeletons, as revealed by the greater

effect-sizes for some of the tests/scales. These results could have important implications

11
for clinical practice, as the costs associated with these two types of RAGT devices are

substantially different.

Notably, severely impaired patients (e.g., FAC score < 2) were not included in

our study because they do not promptly tolerate G-EO training well, unless they are

properly pre-conditioned (13). From a practical standpoint, patients should be initially

stratified according to severity so that the appropriate treatment can be prescribed.

Furthermore, the cost-effectiveness, as well as the risks and contraindications of each

RAGT device should also be taken into account. In a previous publication, we identified

that the main contraindications for RAGT were cardiovascular diseases, skin ulcers and

the presence of spasticity (14). Other authors have reported additional contraindications,

such as use of a cardiac pacemaker, artificial joint replacement in hip/knee joints (up to

two years after implantation), osteoporosis, leg length differences, scoliosis, psychotic

illnesses and body weight greater than 150 kg (13). The adverse events commonly

associated with RAGT have been described in detail by others and include, for instance,

lower limb pain and risk of fracture (5,15).

4.1. Study Limitations

Our findings should be interpreted with caution since they come from a case series type

of study and not from a randomized clinical trial. Thus, we cannot exclude the influence

of allocation bias, even though group assignment was mainly determined by the

scheduling availability of each device, and not by clinical criteria. Besides, assessors

were not blind for the type of RAGT device used by the patients, which might also have

biased our findings. Moreover, all drop-outs were from the G-EO group. Three of these

patients had drop-out reasons likely unrelated to the intervention. The other two patients

were discharged due to knee pain. The exclusion of these two patients from the analyses

12
might have biased our results in favour of the G-EO device, if these patients were to

show no improvements or even deterioration of function due to knee pain. Even though

the RAGT provided by both the exoskeleton and end-effector devices was well

tolerated, with no major side effects, some features of the training with the G-EO device

might have contributed to this problem. However, this issue needs to be addressed in

future studies to confirm this hypothesis. Finally, as we did not perform any adjustments

for multiple comparisons, since our study is exploratory, there is an increased

probability of Type I error in our findings.

Although our study has limitations, its results are important for a better

understanding of the effects of therapies and for planning future studies. Conducting

ancillary studies has been recommended to reduce costs and optimize the benefits of

scientific research data (16).

5. Conclusions

Our results suggest that both end-effectors and exoskeletons may improve clinically

relevant aspects of walking function, as assessed through the tests/scales TUG, DGI,

BBS and ACS. However, this study had a small sample, was retrospective, non-

randomized, and had a significant number of drop-outs, therefore its findings should be

interpreted carefully. Future studies are needed for investigating potential differences in

clinical results, side effects, contraindications and cost effectiveness between these two

different types of RAGT.

Suppliers

a. G-EO System, Reha Technology AG, Switzerland.

b. Lokomat®, Hocoma AG, Switzerland.

13
c. StataCorp LLC, Texas, USA.

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15
Table 1. Demographics of the patients who completed the study.

Lokomat (N=10) G-EO (N=9)

Age (years)
Mean  SD 53.8 ± 13.6 50.5 ± 14
Min, Max 30, 68 31, 79
Gender (%)
Male 30 77.8
Female 70 22.2
Severity (FAC, %)
Mild 60 66.7
Moderate 40 33.3
Stroke type (%)
Ischemic 80 88.9
Hemorrhagic 20 11.1
Stroke time (months)
Mean  SD 17.8 ± 10.96 13.11 ± 9.68
Min, Max 4, 42 4, 30
(< 6 months) 10% 33.3%

16
Table 2. Comparison ‘G-EO Baseline’ vs ‘G-EO Post-training’.

Baseline Post-training Sample

Cohen’s d p-value
(Median, IQ) (Median, IQ) size

TUG 19.4, 13.5,

0.63 0.012 8
(seconds) 12.5 – 33.5 8.5 – 24.9

10MWT 15.4, 12.6,

0.63 0.012 8
(seconds) 10.7 – 33.1 8.6 – 21.6

6MWT 151, 216,

0.63 0.012 8
(meters) 97.5 – 257.3 110.6 – 348.3

16, 17,
TIS 0.50 0.032 9
10 – 17.5 12.5 – 22

12, 16,
DGI 0.63 0.018 7
11 – 15 14 – 17

40.5, 49.5,
BBS 0.63 0.012 8
31.3 – 51.3 44.5 – 55

ACS 14.9, 7.2,

0.63 0.018 7
(seconds) 6.6 – 46.8 5.5 – 21.3

P-values in bold represent statistically significant comparisons.

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Table 3. Comparison ‘Lokomat Baseline’ vs ‘Lokomat Post-training’.

Baseline Post-training Sample

Cohen’s d p-value
(Median, IQ) (Median, IQ) size

TUG 14.7, 13.3,

0.51 0.028 9
(seconds) 11 – 38.5 9.6 – 30.3

10MWT 16.6, 13.7,

0.38 0.129 9
(seconds) 10.4 – 38.2 8.8 – 32.1

6MWT 162.5, 199,

0.38 0.123 8
(meters) 109.6 – 343 165.3 – 414

19, 20,
TIS 0.45 0.056 9
16.5 – 19 17.5 – 21

13.5, 16,
DGI 0.58 0.019 8
10.3 – 21.3 15 – 22.8

44.5, 46.5,
BBS 0.48 0.032 10
33.8 – 51 37.8 – 53.3

ACS 8.4, 8.1,

0.10 0.674 8
(seconds) 4.6 – 14 3.9 – 13.3

P-values in bold represent statistically significant comparisons.

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Table 4. Percentages of participants who had a “real improvement’ (95% CI).

Lokomat (N=10) G-EO (N=9)

TUG (%) 40 (0.12-0.74) 66.7 (0.30-0.93)
10MWT (%) 50 (0.19-0.81) 55.6 (0.21-0.86)
6MWT (%) 50 (0.19-0.81) 77.8 (0.40-0.97)

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