Robotic assisted gait as a tool for rehabilitation of individuals with spinal cord injury: a systematic review
Holanda et al. Journal of NeuroEngineering and Rehabilitation
Robotic assisted gait as a tool for rehabilitation of individuals with spinal cord injury: a systematic review
Ledycnarf J. Holanda 0 3
Patrícia M. M. Silva 0 3
Thiago C. Amorim 0 3
Matheus O. Lacerda 2
Camila R. Simão 1 2
Edgard Morya 0 1 3
0 Neuroengineering Program, Edmond and Lily Safra International Neuroscience Institute, Santos Dumont Institute , Rodovia RN 160, Km 03, 3001 Distrito Jundiaí, Macaíba 59280-000 , Brazil
1 Anita Garibaldi Center of Education and Research in Health, Santos Dumont Institute , Rodovia RN 160, Km 02, 2010 Distrito Jundiaí, Macaíba 59280-970 , Brazil
2 Federal University of Rio Grande do Norte , Av. Sen. Salgado Filho Lagoa Nova, Natal 59078-970 , Brazil
3 Neuroengineering Program, Edmond and Lily Safra International Neuroscience Institute, Santos Dumont Institute , Rodovia RN 160, Km 03, 3001 Distrito Jundiaí, Macaíba 59280-000 , Brazil
Background: Spinal cord injury (SCI) is characterized by a total or partial deficit of sensory and motor pathways. Impairments of this injury compromise muscle recruitment and motor planning, thus reducing functional capacity. SCI patients commonly present psychological, intestinal, urinary, osteomioarticular, tegumentary, cardiorespiratory and neural alterations that aggravate in chronic phase. One of the neurorehabilitation goals is the restoration of these abilities by favoring improvement in the quality of life and functional independence. Current literature highlights several benefits of robotic gait therapies in SCI individuals. Objectives: The purpose of this study was to compare the robotic gait devices, and systematize the scientific evidences of these devices as a tool for rehabilitation of SCI individuals. Methods: A systematic review was carried out in which relevant articles were identified by searching the following databases: Cochrane Library, PubMed, PEDro and Capes Periodic. Two authors selected the articles which used a robotic device for rehabilitation of spinal cord injury. Results: Databases search found 2941 articles, 39 articles were included due to meet the inclusion criteria. The robotic devices presented distinct features, with increasing application in the last years. Studies have shown promising results regarding the reduction of pain perception and spasticity level; alteration of the proprioceptive capacity, sensitivity to temperature, vibration, pressure, reflex behavior, electrical activity at muscular and cortical level, classification of the injury level; increase in walking speed, step length and distance traveled; improvements in sitting posture, intestinal, cardiorespiratory, metabolic, tegmental and psychological functions. Conclusions: This systematic review shows a significant progress encompassing robotic devices as an innovative and effective therapy for the rehabilitation of individuals with SCI.
Robotic assisted gait; Rehabilitation; Robotic devices; Spinal cord injury
In the world, around 250 to 500 thousands people suffer
spinal cord injury (SCI) every year. SCI is caused by a
damage in neural structures of the spinal cord, such as
medulla, medullary cone and/or cauda equina. Tissue
lesions are mostly due to mechanical impact, laceration,
compression, transection, infection or spinal cord
degeneration. SCI is classified in two categories:
incomplete or complete. The first is determined by motor and
sensory partial preservation and reduced
electromyographic (EMG) signal below the injured level, whereas the
second is determined by a complete loss of sensorimotor
activity and EMG signal below the level of lesion [
The sensorial input and motor output are reduced or
absent in SCI patients. Thus, muscular recruitment and
motor planning become compromised, which leads to a
reduced functionality [
]. Chronic SCI patients are
predisposed to secondary complications such as
psychological, bowel, urinary, musculoskeletal, neuronal,
cutaneous and cardiorespiratory [
1, 4, 5
]. Therefore, one
of the challenges in neurorehabilitation to restore
functional independence and quality of life is the recovery of
planning and executing the movement again [
Locomotor functional training is one of the rehabilitation aims
in SCI patients. However, body weight sup- port (BWS)
over a treadmill associated with manual assistance leads to
therapist physical exhaustion. Since the exponential
technological evolution, the idea of improving
rehabilitation, and orthotic devices considering anatomic axes of
lower limb have been developed. This may reduce
professional physical exhaustion and bring new outcomes to
]. As a result, many studies that
investigate the therapeutic effects of these orthotic devices
have been published recently. Several researchers
identified that robotic assisted gait training (RAGT) in SCI
patients improved the cardiorespiratory, urinary,
musculoskeletal, neuronal and somatosensory system, due
to body compensation and neural plasticity [
Therefore, this review aims to compare features, and offer
additional information for robotic devices application, and
systematize scientific evidences from researches which
used these devices as a tool for rehabilitation of SCI
individuals. It is expected that this knowledge compilation
may support further therapies, and researches to improve
organic function and quality of life of SCI patients.
The following databases were searched between February
2016 and October 2017: Cochrane Library, PubMed,
PEDro and Periódico Capes and the manuscript was drafted
from July 2016 to October 2017. To guarantee the most
accurate keywords, it was conducted a search in Medical
Subject Headings (MeSH) with “spinal cord injury”,
“tetraplegic”, “paraplegic”, “lower limbs paralysis” and “lower
extremity paralysis” associated with “body weight
support”, “assisted gait”, “driven gait ortho- sis”, “orthotic gait
training”, “gait training”, “robotic gait”, “exoskeleton”,
“treadmill rehabilitation”, “walking”, “gait”, “locomotion”,
“overground walking”, “robotic assisted gait”, “robotic
assisted gait training”, “treadmill”, “physiotherapy”,
“physical therapy”, “locomotion therapy”, “robotic assisted gait
therapy”, “locomotor treatment”.
Selection of trials
Two authors selected the relevant articles, according
to the following pre-established criteria. Relevant
researches were identified and included only publication
in English, Portuguese and Spanish. Exclusion criteria:
reviews, duplicates and not full article. All papers
which used a robotic device for spinal cord injury
rehabilitation were included independent of the
publication year up to 2017.
Data synthesis and results
The literature search undertaken yielded 2941 records,
of which initially, the titles and abstracts were read and
excluded the duplicate articles. In addition, review
articles and not full text were excluded, resulting in 240
articles. Then, the articles that did not use robotic device
were excluded. Thus, after careful analysis, 39 articles
were included in the full-text review. Figure 1 illustrates
the PRISMA flowchart of the results from the literature
search performed by two authors followed guidelines for
scale’s application as shown.
Table 1 (see Additional file 1: Table 1) shows the
robotic devices and their features e.g. treadmill, BWS,
guidance force (GF), degrees of freedom (DOFs),
maximum pa- tient weight and torso and upper limb muscle
strength, and additional information available in the
reviewed articles. All devices used in the reviewed
articles are pre- sented in Figure 2 with exception of the
Welwalk WW-1000 (K), which has not been published
yet with SCI patient (see Figure: Figure 2). The Figure 3
(see Figure: Figure 3) schematics the increasing use of
robotic devices over the years in rela- tion to the
purpose of their application, highlighting the benefits of
sensorimotor, cardiorespiratory, metabolic, reflex
behavior; kinetic and kinematic parameters.
Further, the tables from two to five contain data from
the articles: study design, patients’ demography,
rehabilitation, outcome measures and results of each article
inserted in this review listed according to the publication
year in ascending order. Moreover, the tables were split
into groups according to outcome measure:
cardiorespiratory and metabolic parameters (Additional file 2: Table
S2), parameters of reflex behavior (Additional file 3:
Table S3), kinetic and kinematic parameters
(Additional file 4: Table S4), and sensory and motors
parameters (Additional file 5: Table S5) (see Additional file 2:
Table S2, Additional file 3: Table S3, Additional file 4:
Table S4, Additional file 5: Table S5, respectively).
Discussion and conclusions
The primary goal of this study was to conduct a
systematic review of scientific evidence related to the use and
features of robotic devices in the rehabilitation of
patients with SCI. From this review, it is possible to base
and guide news prospects for rehabilitation and research,
in view of the numerous benefits that this type of
therapy is able to provide.
Robotic devices are technologies in constant evolution,
e.g. recently was released the Welwalk WW-1000 (L),
which allows pelvis, hip and knee motion for gait
training with BWS and treadmill [
] (see Fig. 2). The
nonstop innovation may offer a paradigm change in the
treatment of individuals with a neurological disorder
]. The exponential technological development lined
Articles found in databases
(n = 2941)
Pubmed (n = 1901)
Periódico Capes (n = 684)
Cochrane Library (n = 300)
PEDro (n = 56)
Full article review (n = 240)
Pubmed (n = 110)
Periódico Capes (n = 30)
Cochrane Library (n = 99)
PEDro (n = 1)
no Do not present robotic
device (n = 201)
Pubmed (n = 86)
Periódico Capes (n = 19)
Cochrane Library (n = 95)
PEDro (n = 1)
Studies included (n = 39)
Pubmed (n = 24)
Periódico Capes (n = 11)
Cochrane Library (n = 4)
PEDro (n = 0)
up with rehabilitation device research is demanding new
addition, the devices cited may be ap- plied in indoor
skills for the rehabilitation professional of the future.
or outdoor environments, considering different DOFs,
The studies included in these review cited features
levels of GF, physical efforts demand and higher
enin relation to the devices, which should be considered
ergy expenditure. The LokomatPRO (plus FreeD
to select the appropriate tool for each individual due
ule) and LOPES are not portable and have as
to the peculiarity of the requirements for its use. In
specification indoor use, BWS and treadmill [
(Donati et al., 2016)
(Walk Again Center, 2015)
(Hartigan et al., 2015)
Lokomat FreeD Module (F)
Pelvic (Hocoma, 2017)
FreeD module) (G)
(BR Biomedicals Pvt. Ltd., 2015)
(Fleerkotte et al., 2014)
(Labini et al., 2014)
(CADTH Evidence Driven, 2015)
(Tanabe, Hirano, Saitoh, 2013)
Welwalk WW-1000 (L)
Fig. 2 Robotic devices used for rehabilitation of individuals with SCI
Whereas the ARGO, EKSO, Indego, Re- Walk and
WPAL can be used either in outdoor and indoor
environments. However, these equipment require high
upper limb load, trunk muscles strength and
excessive energy expenditure due to gait assistance
devices such as crutches or walker to en- sure stability
and safety of the user [
]. Besides possessing
these characteristics, the HAL and Mindwalker
present a controlled activity by bioelectrical signals
detected through surface EMG electrodes measured
in extensor and flexor muscles of the hip and knee
12, 15, 18, 25, 26
]. The EXO does not require
neither muscles strength of upper limbs and trunk, nor
postural control to execute gait and it is flexible to
adjust in a variety of different leg lengths . Thus,
it seems reasonable that robotic gait technology will
merge several features to allow innovative rehabilitation.
Moreover, this review showed that this type of
intervention is able to provide benefits that exceed
improvement of sensorimotor functions of this population.
Figure 3 highlights the applications of robotic devices
for improving sensorimotor, cardiorespiratory and
metabolic parameters until the approaches to altered reflex
behavior, kinetic and kinematic parameters (see Fig. 3).
Among these changes are included, improvements in
activity performance, postural control, urinary and bowel
functions, which are directly related to the
improvements of psychological characteristics and life quality.
The rehabilitation protocol based on specific task
enhances neuroplasticity in individuals with SCI. In this case,
it is important to consider the rehabilitation parameters
used, which should be related to the injury level,
classification, and the secondary changes. During any training
session, the BWS level was selected as the minimum amount
of assistance that would not create excessive knee flexion
during posture or drag during the swing that was
diminished by 5% of BWS. In the inserted studies, initial BWS
was averaged 60% and lasted 45–50%. The weekly
frequency predominance was 2–3 times per week with low
to moderate intensity. The initial treadmill speed varied
between 0.22 and 0.56 m/s and, increased by 0.02 m/s.
Some studies have graded treadmill speed, GF and BWS
according to HR, VO2 and MET of each individual.
Numerous studies revealed changes below the level of
injury with multiple variables observed in the course of
its protocol corroborating with results that indicate
reduced pain perception and spasticity level [
Likewise, it was observed changes in the proprioceptive
ability, sensitivity to temperature, vibration, pressure,
behavior reflex, electrical activity of muscle and cortical
10, 11, 31–44
] and changes in the level of injury
classification. Further, recovery of sensorimotor function;
increased stability and strength of muscles thoracic and
lumbar region [
]; functional improvements in skills in
sitting posture and gait, in the bowel and urinary
function, cutaneous and psychological. Therefore, positively
impacting the performance of their routine activities,
making these individuals with higher level of functional
One study [
] suggests that the RAGT associated
with anabolic medicine does not promote alterations in
bone mineral density (BMD) index, although another
] found divergent results revealing that half of
the participants showed no change while the other half
obtained a small evolution without relation to the
improvement of neurological aspect.
Rehabilitation improvements of an individual with
SCI involves cardiorespiratory fitness, which is
important in improving the quality of life as well as
contributing to a better performance in routine
activities. It was observed that improvements in this
aspect provide a better performance of gait related to
increasing walking speed, stride length, distance
9, 24, 46–49
], related to the reduction of HR,
BF, MET and VO2. Studies [
21, 31, 50, 51
] found a
VO2 and HR variation when compared these
parameters in sitting and orthostatic positions. Further, it
was observed that the higher GF applied to assist
walking, the lower HR and MET, suggesting that the
RAGT interferes in the increase of energy
expenditure, this is capable to provide metabolic and
In conclusion, studies have been able to identify
benefits promoted by the robotic gait devices in SCI
treatments. It is expected in near future that devices should
be used not only during therapy but also in daily living
activities. None the less, the devices should be hybrid
putting together the current SCI individuals abilities and
supporting them where and when their skills lack,
including feedbacks mechanisms to improve the user
benefit from the device. It corroborates to a more individual
centered therapy, based on their specifics needs. Scientific
and technological evidence shows significant progress
encompassing RAGT as an innovative and effective therapy
for the rehabilitation of individuals with SCI, achieving
promising results from improvements in cardiorespiratory,
musculoskeletal, intestinal, urinary, neural, somatosensory
and psychological functions. One of the important features
of this type of treatment is to be a specific therapy based on
motor learning improvements, in which promotes
neuroplasticity and reduce secondary injury complications.
Additional file 1: Table S1. Description of the robotic device(s) used as
a tool for rehabilitation of individuals with SCI. (PDF 157 kb)
Additional file 2: Table S2. Studies that presented metabolic and
cardiorespiratory parameters as outcome measures in individuals with
SCI. (PDF 257 kb)
Additional file 3: Table S3. Studies that presented altered reflex behavior
parameters as outcome measures in individuals with SCI. (PDF 345 kb)
Additional file 4: Table S4. Studies that presented kinetic and kinematic
parameters as outcome measures in individuals with SCI. (PDF 197 kb)
Additional file 5: Table S5. Studies that presented sensory and motors
parameters as outcome measures in individuals with SCI. (PDF 273 kb)
10MWT: 10-meter walk test; 2MWT: 2-minute walk test; 6MWT: 6 min walk
test; ABC: Activities-specific balance confidence; AH: Abductor hallucis;
AIS: American Spinal Injury Association impairment scale; ARGO: Advanced
reciprocating gait orthosis; AROM: Active range of motion; BDI: Beck
depression inventory; BF: Breathing frequency; BFM: Biceps femoris;
BMD: Bone mineral density; BWS: Body weight support; CF: Crutch force;
CG: Control group; COPM: Canadian occupational performance measure;
DELTa: Anterior deltoid; DELTp: Posterior deltoid; DF: Dorsi-flexors;
DGO: Driven gait orthosis; DOFs: Degrees of freedom; DXA: Dual-energy x-ray
absorptiometry; EAW: Exoskeletal - assisted walking; ECU: Extensor carpi
ulnaris; EEG: Electroencephalogram; EG: Experimental group;
EMG: Electromyographic; EXO: FAC: Functional ambulation category;
FCU: Flexor carpi ulnaris; FES-1: Falls efficacy scale; FET: Figure eight scale;
FIM: Functional independence measure; FSR: Force-sensitive resistors;
GF: Guidance force; GMM: Growth mixture modeling; GRC: Gracilis;
GTX: Graded exercise test; HAL: Hybrid assistive limb; HR: Heart rate;
HS: Healthy subject; IPAQ: Impact on participation and autonomy
questionnaire; LEMS: Lower extremity motor score; LH: Lateral hamstrings;
LOA: Level of assistance; LSQ: Life satisfaction questionnaire;
LTSO: Thoracolumbosacral orthosis; MCF: Mean crutch force; MeSH: Medical
Subject Headings; MET: Metabolic equivalents; MG: Medial gastrocnemius;
MH: Medial hamstrings; MVC: Maximal voluntary contraction; P1NP: Intact
aminoterminal propeptide of type I procollagen; PCF: Peak crutch force;
PCI: Physiological cost index; PF: Plantar-flexion; PL: Peroneus longus;
ppSEP: Paired pulse somatosensory evoked potentials; PROM: Passive range
of motion; PTH: Parathyroid hormone; RAGT: Robotic assisted gait training;
RF: Rectus femoris; ROM: Range of motion; RPE: Rate of perceived exertion;
SCI: Spinal cord injury; SCI-FAP: Spinal cord injury-functional ambulation
profile; SCIM: Spinal cord independence measure; SHO: Sides of the acromium;
SOL: Soleus; SpO2: Saturation of peripheral oxygen; SR: Spinal reflex;
ST: Semitendinosus; TA: Tibialis anterior; TLSO: Thoracolumbosacral orthosis;
TUGT: Timed up and go test; UEMS: Upper extremity motor score; VAS: Visual
analog scale; VE: Pulmonary ventilation; VEL: Hip angular velocity; VL: Vastus
lateralis; VM: Vastus medialis; VO2 peak: Peak cardiorespiratory capacity;
VO2: Oxygen uptake; VP: Velocity peak; WISCI II: Walking index for spinal cord
injury II; WPAL: Wearable power-assist locomotor
The authors would like to thank Santos Dumont Institute (ISD), the Brazilian
Ministry of Education (MEC) for their assistance during the research.
LJH reviewed the technical and clinical literature, and drafted the
manuscript. MOL reviewed the technical and clinical literature and drafted
the manuscript. TCO, PMMS, CRS and EM drafted the manuscript. All authors
have read and approved the final manuscript.
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
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