Gait quality is improved by locomotor training in individuals with SCI regardless of training approach
Journal of NeuroEngineering and Rehabilitation
Gait quality is improved by locomotor training in individuals with SCI regardless of training approach
Carla FJ Nooijen 1 2
Nienke ter Hoeve 1 2
Edelle C Field-Fote 0 2
0 Department of Physical Therapy, University of Miami Miller School of Medicine , Miami, FL , USA
1 Faculty of Human Movement Sciences, Research Institute MOVE, VU University , Amsterdam , The Netherlands
2 The Miami Project to Cure Paralysis, University of Miami Miller School of Medicine , Miami, FL , USA
Background: While various body weight supported locomotor training (BWSLT) approaches are reported in the literature for individuals with spinal cord injury (SCI), none have evaluated outcomes in terms of gait quality. The purpose of this study was to compare changes in measures of gait quality associated with four different BWSLT approaches in individuals with chronic motorincomplete SCI, and to identify how gait parameters differed from those of non-disabled (ND) individuals. Methods: Data were analyzed from 51 subjects with SCI who had been randomized into one of four BWSLT groups: treadmill with manual assistance (TM), treadmill with electrical stimulation (TS), overground with electrical stimulation (OG), treadmill with locomotor robot (LR). Subjects with SCI performed a 10-meter kinematic walk test before and after 12 weeks of training. Ten ND subjects performed the test under three conditions: walking at preferred speed, at speed comparable to subjects with SCI, and with a walker at comparable speed. Six kinematic gait quality parameters were calculated including: cadence, step length, stride length, symmetry index, intralimb coordination, and timing of knee extension. Results: In subjects with SCI, all training approaches were associated with improvements in gait quality. After training, subjects with SCI walked at higher cadence and had longer step and stride lengths. No significant differences were found among training groups, however there was an interaction effect indicating that step and stride length improved least in the LR group. Compared to when walking at preferred speed, gait quality of ND subjects was significantly different when walking at speeds comparable to those of the subjects with SCI (both with and without a walker). Post training, gait quality measures of subjects with SCI were more similar to those of ND subjects. Conclusion: BWSLT leads to improvements in gait quality (values closer to ND subjects) regardless of training approach. We hypothesize that the smaller changes in the LR group were due to the passive settings used for the robotic device. Compared to walking at preferred speed, gait quality values of ND individuals walking at a slower speed and while using a walker were more similar to those of individuals with SCI.
Spinal cord injury (SCI) frequently results in paralysis
with subsequent dependence on a wheelchair for
mobility. Recovery of walking function is one of the main
aspirations of these individuals . Different forms of
locomotor training are currently available for individuals
with SCI. One of the most widely used techniques is body
weight supported locomotor training (BWSLT), wherein a
harness/overhead lift system provides partial support to
decrease loading on the lower extremities. During BWSLT
on the treadmill, leg movements are often manually
assisted to aid stepping. According to previous studies,
BWSLT can improve the walking ability of individuals
with chronic motor incomplete paraplegia or tetraplegia
In addition to manual assistance, there are other
approaches available to assist stepping. BWSLT can be
aided by the use of functional electrical stimulation (FES)
while walking on the treadmill or during overground
walking. Despite the emphasis in the literature on the use
of treadmill-based BWSLT, there is evidence from
individuals with both acute  and chronic SCI  that training
overground may be just as effective as training on the
treadmill, while requiring less equipment. FES is used to
activate the muscles or to elicit a spinal reflex response to
promote movements. Previous studies have shown that
the use of FES alone can improve gait in individuals with
SCI [8-11]. The few studies which combined the two
techniques (BWSLT and FES) in individuals with incomplete
SCI were successful in improving walking speed [12,13].
Postans et al.  also found improvements in stride
length, cadence, and gait quality (the latter based on
observational methods). Field-Fote and Tepavac 
identified improvements in intralimb hip-knee
coordination associated with this training approach.
Another approach to assist stepping is combining BWSLT
on the treadmill with robotic assistance. In subjects with
incomplete SCI this form of locomotor training has been
shown to increase walking speed [15,16]. Despite the
many studies that have explored the benefits of different
forms of locomotor training in individuals with SCI, it
remains unclear whether one training approach is
superior for improving walking function in individuals with
The primary purpose of this study is to quantify and
compare changes in gait quality associated with four different
forms of BWSLT in individuals with chronic
motorincomplete SCI. This study is part of a larger project in
which a variety of outcomes associated with the
locomotor training approaches are assessed. In 2005, a
preliminary report of the walking-related outcomes of this study
was published  based on an interim data analysis.
While the sample size at that time was too small to have
sufficient power to detect between-group differences, the
data indicated that all forms of BWSLT studied were
associated with improvements in walking speed. Increases in
step length were found in the groups that trained on the
treadmill in combination with either manual assistance or
FES, and improvements in step symmetry were found in
the groups that trained on the treadmill with either
manual or robotic assistance. In the current account the final
results and between-groups comparisons concerning the
quality of gait are reported. We hypothesized that all
training approaches would be associated with improvements
in gait quality.
A secondary purpose of this article was to compare the gait
quality of individuals with SCI to that of non-disabled
(ND) individuals. Most individuals with chronic
motorincomplete SCI need a walker to be able to walk
overground. Walking with an assistive device can reduce
walking speed, cadence, step length, and stride length [18-23].
Furthermore, in a biomechanical analysis Alkjaer et al.
 showed that walking with a walker can change the
coordination of ND individuals. In ND individuals, we
investigated the effects of walking at a speed comparable
to individuals with SCI, and of walking at this comparable
speed while using a walker, to enable a more accurate
comparison between ND subjects and subjects with SCI.
Subjects with chronic, motor-incomplete SCI were
recruited from the research subject volunteer database at
The Miami Project to Cure Paralysis for participation in a
locomotor training study. A total of 75 subjects
participated over a 5-year period. Inclusion criteria were chronic
SCI defined as injury sustained at least one year prior to
enrollment in the study, the ability to rise from sitting to
standing with at most moderate assistance (50% effort) of
one other person, the ability to advance overground using
an assistive device, and damage to the spinal cord at or
above the level of T12. Individuals with injury below T12
were included only if intact lower motor neuron function
could be confirmed by brisk reflex responses to
quadriceps, tibialis anterior, and soleus reflex testing. Exclusion
criteria were current orthopedic problems, history of
cardiac conditions, and presence of active hip pathology that
could be aggravated by the training (e.g. severe
osteoarthritis, heterotopic ossification). All subjects were
medically cleared by the study physiatrist prior to participation.
In addition, 10 ND subjects with no known orthopedic or
neurological deficits were included for comparison of gait
parameters. All subjects gave written informed consent
according to the guidelines established by the Office of
Human Subjects Research at the University of Miami,
Miller School of Medicine.
Subjects with SCI were stratified into one of four levels
based on their pre-training lower extremity strength as
measured by lower extremity motor score (LEMS). The
LEMS represents the sum of the scores on the manual
muscle strength test for five lower extremity key muscles
as defined in the international standards for neurological
classification of spinal cord injury . The stratification
levels were Stratum 1 = LEMS of 1 - 10; Stratum 2 = LEMS
of 11- 21; Stratum 3 = LEMS of 22 - 32; Stratum 4 = LEMS
of >32. Subjects within each stratum were then randomly
assigned to one of four training groups. The training
groups were: (1) BWSLT on the treadmill with manual
assistance for stepping (TM), (2) BWSLT on the treadmill
with peroneal nerve stimulation to assist stepping (TS),
(3) BWSLT overground with peroneal nerve stimulation
(WalkAide2™, Hanger Orthopedic Group, Inc., Bethesda,
MD; OG), and (4) BWSLT on the treadmill with assistance
of a locomotor robot (Lokomat, Hocoma AG, Zurich,
Switzerland; LR). The amount of weight support was
adjusted within and between sessions as needed to
prevent excessive knee flexion during stance phase or toe
dragging during swing phase. Support was maintained at
or below 30% (with the exception of a few subjects who
needed more support during the first week of training), as
this level of support is associated with gait kinematics
which resemble unsupported walking . Subjects in the
first three groups (TM, TS, and OG) were encouraged to
walk at their maximum possible speed at which step
kinematics were acceptable (no toe dragging, an adequate
knee flexion during swing phase, adequate knee extension
at initial stance phase, etc). Subjects in the TM group
received assistance for stepping based on guidelines
recommended by Behrman and Harkema . Subjects in
the TS group received bilateral stimulation (Digitimer Ltd,
Hertfordshire, UK) to the common peroneal nerve at a
stimulus intensity intended to elicit a flexion withdrawal
response according to procedures we have previously
reported [12,14]. Subjects in the LR group walked at a
speed of 2.6 km/h and speed was increased by 0.16 km/h
each week with a goal of reaching the maximum device
speed of 3.2 km/h. The robotic training protocol was one
of passive mechanical guidance as the option to decrease
the guidance forces (allowing the subject to move against
the machine) was not available at the time the study was
initiated. All subjects were allowed to rest as needed
during the training sessions. Subjects trained 5 days per week
for 12 weeks in daily sessions of 60 minutes (15 minutes
of subject preparation, 45 minutes of training). None of
the subjects was involved in other training activities. For
more details about the training procedures see published
preliminary report .
Subjects with SCI performed a 10-meter walk test. During
this test, kinematic data were captured within the central
6 meters of the walkway using an 8-camera infrared
system (Vicon Peak™, Englewood, CO), with a 60 Hz capture
rate. A total of 21 reflective markers were placed bilaterally
at the lateral malleoli, 5th ray metatarsal-phalangeal joints,
heels, lateral knee joints, greater trochanters, anterior
superior iliac spines, shoulders, elbows, and wrists as well
as at C7, T10, and the sacrum. Subjects with SCI walked
across the walkway five times with the instruction to walk
at their fastest comfortable walking speed, and were
allowed to rest between bouts. Comfortable walking
speed was chosen since we believe this is most
representative of everyday performance, and therefore reflects the
real-world relevance of training-related changes in
function. Subjects used the upper extremity assistive devices,
and if necessary lower extremity orthotic devices, with
which they were most familiar. Subjects used the same
assistive device during the initial and final test sessions.
Walk tests were performed without support for body
weight or assistance for stepping. Analysis of the
kinematic data was performed by two of the authors (CN and
NH) who were not otherwise involved in the study.
ND subjects performed the 10-meter walk test in three
different conditions on a single occasion: (1) at their
preferred walking speed (PS), (2) at a walking speed
comparable to subjects with SCI (0.3 m/s; CS), and (3) at
a walking speed comparable to subjects with SCI (0.3 m/
s) while using a walker (WCS). Each subject performed
three trials of each condition, which is thought to be
sufficient as little variation is expected in the walking
performance of ND subjects.
Kinematic data were filtered using a low-pass Butterworth
filter (cutoff frequency= 6 Hz). A total of six parameters
related to gait quality were calculated from the kinematic
data: cadence (CAD), step length (STEP), stride length
(STRIDE), symmetry index (SI), intralimb coordination
(ACC), and timing of knee extension onset within the hip
CAD (steps/minute) was determined by the total number
of steps divided by the time needed to complete these
steps. STEP (m) of the leading leg was defined as the
distance between two consecutive contralateral heel strikes.
The five longest steps of each leg were selected out of all
trials and these five steps were averaged for statistical
analysis. The stronger leg was operationally defined as the leg
that, on average, made the longest steps during the initial
test for subjects with SCI, and during walking at preferred
walking speed (PS) for ND subjects. The opposite leg was
defined as the weaker leg. Step lengths were normalized to
leg length. Leg length was calculated by adding the
segmental lengths of thigh, shank, and the distance of the
malleoli to the floor during stance phase of gait. STRIDE
(m) was based on the five longest steps of each leg. The
normalized lengths of the steps that preceded the five
longest steps were added to the normalized longest step
lengths for both the stronger and weaker leg.
within-subject factor was testing session (initial and
final). Training, group, and interaction effects were further
analyzed using post hoc tests with Bonferroni correction.
Bilateral step symmetry was calculated using the
symmetry index  according to equation 1:
where SLs is step length of the stronger leg and SLw is step
length of the weaker leg.
A SI-value of zero represents perfect symmetry between
legs. Absolute SI values were used for statistical analysis.
Intralimb coordination was defined as the ability to
produce a consistent intralimb coupling relationship
between knee angle and hip angle over multiple step
cycles. This measure offers insights into the organization
of control mechanisms underlying the coordination of
walking [14,29]. The knee angle was defined as the angle
formed by thigh and shank segments, and the hip angle
was defined as the angle formed by trunk and thigh
segments. Overall variability in the relationship between
knee angle and hip angle was represented by the angular
component of the coefficient of correspondence (ACC)
which was calculated by using the vector coding
technique . An ACC value closer to 1 represents a greater
consistency between knee-hip cycles. ACC values were
calculated for both the stronger and weaker leg.
Timing of knee extension onset within the hip cycle was
calculated to determine if the knee-hip coordination
pattern in subjects with SCI is comparable to that of ND
subjects. This is necessary since consistent intralimb coupling
(i.e. high ACC values) of subjects with SCI do not
necessarily represent a movement pattern that resembles that of
ND subjects. The hip cycle was defined as the time from
onset of hip flexion to the onset of the subsequent hip
flexion. Within this normalized cycle, the phase value of
the first knee extension onset (i.e. that occurring at
approximately mid-swing) was calculated . For the
subjects with SCI, values closer to those obtained for ND
subjects were considered representative of better gait
The statistical analysis of STEP and STRIDE data was based
on the average of the five longest steps of each leg. For all
other variables, the average of all trials was used for
analysis. Statistical analysis was performed using SPSS version
17.0. The level of significance was set at p < 0.05. A
twoway repeated measures analysis of variance (ANOVA) was
performed to compare gait parameters. The
between-subject factor was group (TM, TS, OG, and LR) and the
A one-way repeated measures ANOVA was used for
analyzing the data of the ND subjects with condition (PS, CS,
and WCS) as a within-subject factor. Condition main
effects were further analyzed using post hoc tests with
Finally, a one-way ANOVA was used to compare both the
initial and final testing sessions of subjects with SCI with
the WCS condition of ND subjects.
For the consideration of sphericity in all analyses, the
Huyn-Feldt corrected value was used if
GreenhouseGeisser epsilon was larger than 0.75. Otherwise, the
Greenhouse-Geisser corrected value was used to correct
degrees of freedom in the analysis . For the repeated
measures ANOVA, estimates of the effect sizes for the
main and interaction effects were represented by partial
η2 (pη2). The exact effect size (η2) was calculated for the
one-way ANOVA's. The effect size describes the
percentage of variance which is explained in the dependent
variable by a predictor while controlling for other predictors
A total of 51 subjects with SCI were included for analysis.
Data of 24 subjects (assigned to the following groups: TM
= 6, TS = 7, OG = 7, LR = 4) were excluded for analysis for
the following reasons: 10 subjects were unable to achieve
a kinematically identifiable step during initial testing, 10
subjects withdrew from the study for personal reasons or
medical reasons not related to the study, and data
collection failed due to technical difficulties for 4 subjects.
Although not included in the analysis, it is noteworthy
that of the 10 subjects who were unable to achieve a step
during initial testing, 4 were able to take steps during the
final test session.
The mean number of training sessions completed by the
subjects with SCI over the 12-week training period was 50
(SD = 6.57, range = 30-58). A total of 42 subjects with SCI
walked with a walker, 3 with a cane, and 6 with forearm
crutches. The stratified randomization into the four
different training groups resulted in the following subject
distribution: TM = 13, TS = 15, OG = 11, LR = 12. Additional
descriptive information can be found in Table 1. The ND
subject group consisted of 5 men and 5 women with a
mean age of 26.5 years (SD = 9.87, range = 22-54).
Complete data sets were available to calculate STEP, CAD
and SI for all included subjects. STRIDE data were (partly)
Gender Chronicity (months) Level of injury Group Age
Gender Chronicity (months) Level of injury
missing for six subjects with SCI as an insufficient number
of strides were recorded. Complete data sets for ACC were
available for 38 subjects and TOK data for 27 subjects. For
ten subjects with SCI included in analysis we were not
able to calculate ACC and TOK as not all angle data were
available. Furthermore, for three other subjects ACC and
TOK could not be determined, since an insufficient
number of steps were recorded during the initial
measurement. For an additional 11 subjects TOK data were
(partly) missing, because the knee extension or hip
flexion maxima could not be determined from the angle data.
Training effects in subjects with SCI
No significant between-group differences were found for
any of the parameters, indicating that the gait parameters
of interest were comparable between the different training
groups, both before training and after training. Therefore
pooled data of the subjects with SCI were used to assess
effects of training on the selected measures of gait quality.
Main effects of training were identified for cadence (F
(1,47) = 14.51, p < 0.01, pη2 = 0.24), step length of the
stronger (F(1,47) = 14.00, p < 0.01, pη2 = 0.23) and weaker
leg (F(1,47) = 25.05, p < 0.01, pη2 = 0.35), and stride
length of the stronger (F(1,47) = 11.09, p < 0.01, pη2 =
0.20) and weaker leg (F(1,47) = 20.21, p < 0.01, pη2 =
0.32) (see Figure 1A, B, C). Following training, subjects in
all groups were, on average, able to take more steps per
minute (pre-post difference: TM = 2.3 steps/min, TS = 3.9
steps/min, OG = 5.0 steps/min, LR = 1.5 steps/min). The
step and stride lengths of the subjects in the LR group did
not differ more than 0.01 m between pre- and
post-training, while subjects in the other groups were able to take
longer steps with the stronger leg (pre-post difference: TM
= 0.03 m, TS = 0.06 m, OG = 0.10 m) and weaker leg
(prepost difference: TM = 0.07 m, TS = 0.12 m, OG = 0.09 m),
as well as take a longer stride with the stronger leg
(prepost difference: TM = 0.07 m, TS = 0.07 m, OG = 0.10 m)
and weaker leg (pre-post difference: TM = 0.08 m, TS =
0.08 m, OG = 0.16 m).
Interaction effects were identified for step length (both
strong and weak) and stride length of the weaker leg,
therefore, post-hoc analyses were performed. These
analyses revealed that subjects in the OG group had a
significantly larger gain compared to subjects in the LR group in
step length of the stronger leg (mean difference = 0.11 m,
p = 0.01) and in stride length of the weaker leg (mean
Gait parameters of subjects with SCI before and after the four different forms of body weight supported
locomotor training (TM = manual assistance, TS = peroneal nerve stimulation, OG = overground with peroneal
nerve stimulation, LR = robotic assistance), and gait parameters of non disabled subjects during the condition
in which they walked at a slow speed while using a walker. Error bars represent standard deviation and n represents
the number of individuals with SCI included in analysis of each parameter. CAD = cadence, SI = symmetry index, ACC =
angular component of coefficient of correspondence, TOK = timing of knee extension onset.
ference = 0.16 m, p = 0.04). Subjects in the TS group
showed a significantly larger gain compared to subjects in
the LR group in step length of the weaker leg (mean
difference = 0.12 m, p = 0.02).
No main training effects were found for symmetry index,
intralimb coordination (of the stronger and weaker leg),
and timing of knee extension onset (of the stronger and
weaker leg) (see Figure 1D, E, F). The lack of statistical
improvement in intralimb coordination and timing of
knee extension onset could be related to the smaller
sample sizes for these parameters due to missing data (see
Figure 1). However, as will be discussed in a subsequent
section, timing of knee extension onset prior to training
was not different from that of ND subjects; therefore
changes in this measure would not be expected.
Effects of different walking conditions in ND subjects
Main effects of walking condition were found for cadence,
step length (strong and weak), and stride length (strong
and weak). Compared to walking at preferred speed (PS),
ND subjects took, on average, fewer steps per minute in
the CS condition wherein the mean difference was 37.89
steps/minute, and fewer steps per minute in the WCS
condition wherein the mean difference was 38.61 steps/
minute (CAD; F(2,18) = 5.76, p < 0.01, pη2 = 0.91). On
average ND subjects took shorter steps with the stronger
leg in the CS and WCS condition; the mean difference
with the PS condition was 0.26 m for each (STEP_strong;
F(2,18) = 115.72, p < 0.01, pη2 = 0.93). ND subjects also
took shorter steps with the weaker leg wherein mean
difference with the PS condition was 0.25 m for the CS
condition and 0.24 m for the WCS condition (STEP_weak;
F(2,18) = 87.25, p < 0.01, pη2 = 0.91). Compared to the PS
condition, on average ND subjects took shorter strides
with the stronger leg in both the CS and WCS condition
wherein mean difference was 0.51 m for each
(STRIDE_strong; F(2,18) = 87.43 p < 0.01, pη2 = 0.91). ND
subjects also took shorter strides with the weaker leg in the
CS condition wherein mean difference was 0.54 m, and in
the WCS condition wherein mean difference was 0.50 m
(STRIDE_weak; F(2,18) = 104.48, p < 0.01, pη2 = 0.92).
Main effects of condition were also identified for step
symmetry, intralimb coordination (strong and weak), and
timing of knee extension onset (strong and weak).
Bilateral step symmetry was significantly smaller in the WCS
condition (mean difference = 2.84) and CS condition
(mean difference = 1.96) compared to the PS condition
(SI; F(2,18) = 5.76, p = 0.01, pη2 = 0.39). Intralimb
coupling of the stronger and weaker leg was less consistent in
the CS (mean difference for each leg = 0.04) and WCS
condition (mean difference for each leg = 0.03) compared
to the PS condition (ACC_strong; F(2,18) = 13.14, p <
0.01, pη2 = 0.59 and ACC_weak; F(2,18) = 13.56 p < 0.01,
pη2 = 0.60). Timing of knee extension onset of the stronger
leg occurred earlier in the CS condition than in the PS
condition with a mean difference of 0.04% of cycle
(TOK_strong; F(2,18) = 9.73, p < 0.01, pη2 = 0.52). Timing
of knee extension onset of the weaker leg occurred earlier
in both the CS (mean difference = 0.03% of cycle) and
WCS condition (mean difference = 0.04% of cycle)
compared to the PS condition (TOK_weak; F(2,18) = 11.60, p
< 0.01, pη2 = 0.56).
Comparison between subjects with SCI and ND subjects
Gait quality values of subjects with SCI were compared to
values of ND subjects walking in the WCS condition. The
WCS condition was chosen as it is most similar to the
walking condition of individuals with SCI. This enables a
better comparison between ND subjects and subjects with
SCI, since results indicated that a reduced speed and the
use of a walker can influence gait quality.
Subjects with SCI had a cadence that was significantly
lower than that of ND subjects walking in the WCS
condition (see Figure 1A). Subjects with SCI took on average
13.44 fewer steps/minute in the initial test, and 10.28
fewer steps/minute in the final test compared to the ND
subjects (initial test; F(1,59) = 8.99, p < 0.01, η2 = 1.88 and
final test; F(1,59) = 4.96, p = 0.03, η2 = 1.44). In the initial
test subjects with SCI took steps with the weaker leg that
were on average 0.12 m shorter than the steps of the ND
subjects (F(1,59) = 5.9, p = 0.02, η2 = 2.34). During the
final test this difference was no longer significant (F(1,59
= 0.92, p = 0.34, η2 = 1.02). No significant differences were
found between subjects with SCI and ND subjects for step
length of the stronger leg, and for stride length of both the
stronger and weaker leg (see Figure 1B, C).
Bilateral step symmetry was significantly lower for
subjects with SCI, compared to ND subjects during the initial
test as indicated by larger SI values for the subjects with
SCI (mean difference = 33.45, F(1,59) = 4.88, p = 0.03, η2
= 11.33). After training, there was no longer a significant
difference in SI between subjects with SCI and ND
subjects (F(1,59) = 3.42, p = 0.07, η2 = 8.30) (see Figure 1D).
The initial intralimb coordination values differed
significantly between subjects with SCI and ND subjects for both
the stronger leg (F(1,59) = 43.58 p < 0.01, η2 = 13.45) and
the weaker leg (F(1,59) = 32.09 p < 0.01, η2 = 9.73). There
remained a difference between ND subjects and subjects
with SCI during the final test for both the stronger leg
(F(1,59) = 26.24, p < 0.01, η2 = 13.20) and the weaker leg
(F(1,59) = 25.01, p < 0.01, η2 = 10.08). ND subjects had a
more consistent intralimb coupling during the pre (mean
ACC difference = 0.27) and post test (mean ACC
difference = 0.26) for the stronger limb and during the pre
(mean ACC difference = 0.25) and post test (mean ACC
difference = 0.26) for the weaker limb (see Figure 1E).
No significant differences between subjects with SCI and
ND subjects were found for the timing of knee extension
onset at the time of the initial or final test (see Figure 1F).
Training effects in subjects with SCI
When selecting a locomotor training approach for
individuals with chronic SCI, the therapist may decide to give
primary attention to an approach that focuses on
improving gait quality. In such cases the results of this study
indicate that there are several options, as all four BWSLT
approaches were associated with improvements in
variables associated with gait quality and no significant
differences among groups were found.
This is the first article with a main focus on improvements
in gait quality after locomotor training in individuals with
chronic SCI. Across training groups subjects with SCI
showed significant improvements in cadence, step length
and stride length. The data indicated that, on average,
increases in step length were larger for the weaker leg
compared to the stronger leg, which could be related to the
(non-significant) increase in the bilateral step symmetry.
The large variation observed in the step symmetry of
subjects with SCI could be the reason that this increase was
not statistically significant (see Figure 1D). In individuals
with acute SCI Postans et al.  also found increases in
cadence and stride length after BWSLT combined with
electrical stimulation. Since individuals in that study were
trained during the acute phase of SCI, it is likely that part
of the observed improvements may have been due to the
spontaneous recovery that occurs in the first post-injury
year. Improvements in step and stride length were also
found after locomotor training with electrical stimulation
without body weight support [9,11]. Furthermore, in
individuals with stroke, BWSLT has shown to be effective
in improving gait quality [3,32-38]. Since there is a
considerable variability in training protocol, intensity, and
subjects among the studies, it is complicated to make a
good comparison between the amounts of improvement.
Therefore, more research is necessary about the specific
influences of training parameters .
Regardless of the approach, BWSLT leads to
improvements in gait quality. This conclusion is in accordance
with a recent review of Merholz et al.  in which it was
concluded that the different forms of locomotor training
used in the present study are all effective in improving
walking speed and capacity. However, group effects could
have been masked in the current study, since there was a
large variation among subjects within the different
training groups for all parameters, in part because the study
design was intended to include both higher and lower
functioning subjects in each group. This large variation
could have accounted for an overlap in outcomes between
groups (see Figure 1).
Subjects who received electrical stimulation (TS and OG
group) improved step and stride length to a greater extent
than subjects who were trained with robotic assistance
(LR group). The LR group showed no or only slight
increases in step and stride length, while the other training
groups improved substantially on these parameters. Also,
mean changes in bilateral step symmetry tended to favor
the other three training approaches above LR. It is
essential to note however, that in the present study the robotic
training protocol did not include the option to decrease
the guidance forces and require the subject to exert effort,
as this option was not available on the device at the time
this study was initiated. Although subjects in the LR group
were encouraged to "walk with the machine," it is likely
that these subjects did not exert the level of voluntary
effort that was exerted by subjects in the other groups.
These results may indicate that voluntary effort is
important for developing the motor skills required for
improvements in gait quality. The results also suggest that BWSLT
combined with passive mechanical guidance is not the
preferable training approach for improving gait quality in
individuals with chronic SCI. However, this training
approach could be more effective for subjects with more
severely impaired locomotor function. Furthermore, the
use of the more active Lokomat training protocol, using
software that was not available at the time this study was
initiated, might lead to other results, and further research
is necessary to find the optimal set of training parameters
for walking with robotic assistance .
For all training approaches, locomotor training did not
lead to a more consistent coordination between limbs and
the timing of knee extension onset was not altered by
training. These results are in contrast to the outcomes of a
study of Field-Fote et al.  in which the consistency of
the intralimb coordination in subjects with SCI increased
and the timing of knee extension onset was earlier in the
hip cycle following locomotor training. Difference in
training and testing procedures between the two studies
may explain differences in findings. In the study by
FieldFote et al. , subjects were trained and tested on a
treadmill. In the present study three of the four groups were
trained on the treadmill, while the gait analyses were all
performed overground. According to Alton et al ,
comparison of overground and treadmill gait analyses
should be avoided in patients. Significant differences in
hip and knee motion variables are found between
overground and treadmill walking in several studies [41-44].
The finding that timing of knee extension onset of
subjects with SCI was not different from that of the ND
subjects in the present study wherein testing was based on
overground walking, but was different in a similar group
of subjects wherein testing was based on treadmill
walking , suggests that the walking environment
influences the gait parameters related to coordination. The
finding of no change in intralimb coordination in subjects
who (for the most part) were trained on the treadmill but
tested overground, may reflect incomplete transfer of
motor learning underlying the control of coordination
from the treadmill to the overground condition.
Different walking conditions in ND subjects
When the ND subjects walked both with and without a
walker (WCS and CS condition) at a speed that was
comparable to that of individuals with SCI, they took fewer
steps per minute and decreased the length of their steps
and strides. This modification of cadence, and step and
stride length is typical of ND individuals when they desire
to adjust walking speed . Furthermore, walking at this
speed resulted in a less consistent intralimb coordination.
This is in accordance with previous research in which
correlations between speed and intralimb coordination were
found [14,46,47]. Finally, during walking at reduced
speed, the onset of first knee extension occurred later in
the hip cycle. Our finding that gait quality changes when
walking at reduced speeds regardless of whether a walker
was used, suggests that prior studies wherein a reduction
in gait quality has been attributed to the use of the
assistive device [18-23], the reduced gait quality may not
reflect a direct result of the use of an assistive device.
Rather, it is likely that the assistive device caused the ND
individuals to reduce their speed, which indirectly
resulted in reduced gait quality.
In addition to the changes in intralimb coordination that
accompanied walking at reduced speeds (with and
without a walker) in ND individuals, walking with a walker
resulted in less symmetry of bilateral stepping. For the
condition in which subjects only walked at a reduced
speed (without a walker), the step symmetry was
comparable to that when walking at preferred speed. This
indicates that the use of an assistive device can change the
symmetry between the limbs.
These results suggest that when attempting to identify
how the gait quality of individuals who walk at a reduced
speed and require an assistive device (such as those with
SCI) differs from "normal" gait, walking speed may have
a greater influence on these parameters than the use of the
assistive device. However, this should not be construed to
suggest that the walking speed during locomotor training
is the critical factor in improving walking function, as our
prior work indicates that those who train at slower speeds
while walking overground make improvements in
walking function that are, in some cases, greater than those
experienced by individuals who train at faster speeds on
the treadmill .
Comparison between subjects with SCI and ND subjects
Following three months of daily locomotor training,
several parameters of the gait quality of subjects with SCI
improved such that it became more similar to the gait
quality of ND subjects. The mean difference in cadence
between ND subjects and subjects with SCI during the
final test was smaller compared to the mean difference
during the initial test. The significant shorter step length
of the weaker leg and the bilateral step asymmetry that
subjects with SCI exhibited at the initial test were no
longer present at the time of the final test, and these gait
parameters were comparable to those of the ND subjects.
Step length of the stronger leg and stride length were
already comparable between subjects with SCI and ND
subjects at the start of training. No differences were found
for timing of knee extension onset in the hip cycle.
As stated previously, the large amount of variability in all
outcome parameters of subjects with SCI may be
responsible for the lack of significant findings related to some of
the parameters of interest. The large variability is likely
due to differences in the degree of injury among subjects.
However, variability is a well-known and mostly
insurmountable problem in studies of individuals with
Furthermore, a large number of subjects were excluded
from the analyses either because the individual was
unable to achieve a step that was kinematically identifiable,
withdrew from the study, or the kinematic data set was
incomplete. The lack of an intention-to-treat analysis is a
limitation of this study. The number of subjects excluded
due to lack of a kinematically identifiable step (n = 10) or
because of incomplete kinematic data (n = 4) may have
been lower if testing had been repeated on multiple days.
Since individuals with SCI have a day-to-day variation in
standing performance and ability to walk, a larger amount
of within-subject baseline data would likely have reduced
the variability in outcome parameters. In addition, some
of the subjects who were unable to take any steps may
have been able to make an identifiable step during at least
one of the test days with repeated testing. However, given
that at least three steps on each side are required to make
meaningful conclusions about gait quality, and since only
four out of ten of these subjects were able to take steps
after training, repeated testing may not have made a large
difference in the data for this subgroup of subjects.
This study assessed only locomotor training approaches
that used partial support for body weight. It is not known
how these results compare to outcomes of locomotor
training wherein support for body weight is not provided.
Results in individuals with acute SCI appear to indicate
that support for body weight is not a critical factor . It
is also possible that a combination of treadmill-based
BSWLT and overground training without body weight
support may be the optimal approach . However,
direct comparisons must be made in individuals with
chronic SCI before definitive conclusions can be reached.
Regardless of training approach, gait quality improved in
individuals with chronic motor-incomplete SCI following
BWSLT, such that the values became more similar to those
of ND individuals. The greatest improvement in gait
quality was found for subjects who trained with electrical
stimulation. Less improvement was found for individuals who
trained with passive robotic assistance. Furthermore,
when ND subjects were walking at a reduced speed and
when they were using a walker, their gait quality values
changed and became more comparable to those of
individuals with SCI.
Based on the results of this study, therapists can be
confident that practice in walking is the key element for the
success of a BWSLT program wherein the goal is to improve
gait quality in individuals with chronic motor-incomplete
SCI. Furthermore, when comparing gait quality values of
individuals who walk at a reduced speed and require an
assistive device (such as those with SCI) and ND
individuals, it is advised to use data in which ND subjects walk at
a reduced speed while using a walking device.
The authors declare that they have no competing interests.
NH and CN performed the data analysis of all subjects,
measurements of healthy subjects, statistical analysis, and
drafted the manuscript. EF participated in the design,
execution, and coordination of the study and assisted with
drafting the manuscript. All authors read and approved
the final manuscript.
Support for this project was provided by the National Institutes of Health
(R01HD41487), by the National Institute on Disability and Rehabilitation
Research (H133B031114), by the Schumann Foundation, and by The Miami
Project to Cure Paralysis. We thank the staff of the Neuromotor
Rehabilitation Research Laboratory of The Miami Project to Cure Paralysis and
Thomas Janssen (VU University) for their support.
1. Lapointe R , Lajoie Y , Serresse O , Barbeau H : Functional community ambulation requirements in incomplete spinal cord injured subjects . Spinal Cord 2001 , 39 : 327 - 335 .
2. Protas EJ , Holmes SA , Qureshy H , Johnson A , Lee D , Sherwood AM : Supported treadmill ambulation training after spinal cord injury: a pilot study . Arch Phys Med Rehabil 2001 , 82 : 825 - 831 .
3. Visintin M , Barbeau H : The effects of body weight support on the locomotor pattern of spastic paretic patients . Can J Neurol Sci 1989 , 16 : 315 - 325 .
4. Wernig A , Muller S , Nanassy A , Cagol E : Laufband therapy based on 'rules of spinal locomotion' is effective in spinal cord injured persons . Eur J Neurosci 1995 , 7 : 823 - 829 .
5. Wernig A , Nanassy A , Muller S : Maintenance of locomotor abilities following Laufband (treadmill) therapy in para- and tetraplegic persons: follow-up studies . Spinal Cord 1998 , 36 : 744 - 749 .
6. Dobkin B , Barbeau H , Deforge D , Ditunno J , Elashoff R , Apple D , et al.: The evolution of walking-related outcomes over the first 12 weeks of rehabilitation for incomplete traumatic spinal cord injury: the multicenter randomized Spinal Cord Injury Locomotor Trial . Neurorehabil Neural Repair 2007 , 21 : 25 - 35 .
7. Field-Fote EC , Lindley SD , Sherman AL : Locomotor training approaches for individuals with spinal cord injury: a preliminary report of walking-related outcomes . J Neurol Phys Ther 2005 , 29 : 127 - 137 .
8. Barbeau H , Ladouceur M , Mirbagheri MM , Kearney RE : The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies . Brain Res Brain Res Rev 2002 , 40 : 274 - 291 .
9. Johnston TE , Finson RL , Smith BT , Bonaroti DM , Betz RR , Mulcahey MJ : Functional electrical stimulation for augmented walking in adolescents with incomplete spinal cord injury . J Spinal Cord Med 2003 , 26 : 390 - 400 .
10. Ladouceur M , Barbeau H : Functional electrical stimulationassisted walking for persons with incomplete spinal injuries: longitudinal changes in maximal overground walking speed . Scand J Rehabil Med 2000 , 32 : 28 - 36 .
11. Wieler M , Stein RB , Ladouceur M , Whittaker M , Smith AW , Naaman S , et al.: Multicenter evaluation of electrical stimulation systems for walking . Arch Phys Med Rehabil 1999 , 80 : 495 - 500 .
12. Field-Fote EC : Combined use of body weight support, functional electric stimulation, and treadmill training to improve walking ability in individuals with chronic incomplete spinal cord injury . Arch Phys Med Rehabil 2001 , 82 : 818 - 824 .
13. Postans NJ , Hasler JP , Granat MH , Maxwell DJ : Functional electric stimulation to augment partial weight-bearing supported treadmill training for patients with acute incomplete spinal cord injury: A pilot study . Arch Phys Med Rehabil 2004 , 85 : 604 - 610 .
14. Field-Fote EC , Tepavac D : Improved intralimb coordination in people with incomplete spinal cord injury following training with body weight support and electrical stimulation . Phys Ther 2002 , 82 : 707 - 715 .
15. Hornby TG , Zemon DH , Campbell D : Robotic-assisted, bodyweight-supported treadmill training in individuals following motor incomplete spinal cord injury . Phys Ther 2005 , 85 : 52 - 66 .
16. Wirz M , Zemon DH , Rupp R , Scheel A , Colombo G , Dietz V , et al.: Effectiveness of automated locomotor training in patients with chronic incomplete spinal cord injury: a multicenter trial . Arch Phys Med Rehabil 2005 , 86 : 672 - 680 .
17. Mehrholz J , Kugler J , Pohl M : Locomotor training for walking after spinal cord injury . Spine 2008 , 33 : E768 - E777 .
18. Ely DD , Smidt GL : Effect of cane on variables of gait for patients with hip disorders . Phys Ther 1977 , 57 : 507 - 512 .
19. Foley MP , Prax B , Crowell R , Boone T : Effects of assistive devices on cardiorespiratory demands in older adults . Phys Ther 1996 , 76 : 1313 - 1319 .
20. Li S , Armstrong CW , Cipriani D : Three-point gait crutch walking: variability in ground reaction force during weight bearing . Arch Phys Med Rehabil 2001 , 82 : 86 - 92 .
21. Opila KA , Nicol AC , Paul JP : Forces and impulses during aided gait . Arch Phys Med Rehabil 1987 , 68 : 715 - 722 .
22. Smidt GL , Wadsworth JB : Floor reaction forces during gait: comparison of patients with hip disease and normal subjects . Phys Ther 1973 , 53 : 1056 - 1062 .
23. Youdas JW , Kotajarvi BJ , Padgett DJ , Kaufman KR : Partial weightbearing gait using conventional assistive devices . Arch Phys Med Rehabil 2005 , 86 : 394 - 398 .
24. Alkjaer T , Larsen PK , Pedersen G , Nielsen LH , Simonsen EB : Biomechanical analysis of rollator walking . Biomed Eng Online 2006 , 5 : 2 .
25. Mulcahey MJ , Gaughan J , Betz RR , Vogel LC : Rater agreement on the ISCSCI motor and sensory scores obtained before and after formal training in testing technique . J Spinal Cord Med 2007 , 30 (Suppl 1): S146 - S149 .
26. Finch L , Barbeau H , Arsenault B : Influence of body weight support on normal human gait: development of a gait retraining strategy . Phys Ther 1991 , 71 : 842 - 855 .
27. Behrman AL , Harkema SJ : Locomotor training after human spinal cord injury: a series of case studies . Phys Ther 2000 , 80 : 688 - 700 .
28. Galea MP , Levinger P , Lythgo N , Cimoli C , Weller R , Tully E , et al.: A targeted home- and center-based exercise program for people after total hip replacement: a randomized clinical trial . Arch Phys Med Rehabil 2008 , 89 : 1442 - 1447 .
29. Tepavac D , Field-Fote EC : Vector coding: A technique for quantification of intersegmental coupling in multicyclic behaviors . Journal of Applied Biomechanics 2001 , 17 : 259 - 270 .
30. Girden E : ANOVA: Repeated Measures Sage ; 1992 .
31. Cohen J : Eta-Squared and Partial Eta-Squared in Fixed Factor Anova Designs . Educational and Psychological Measurement 1973 , 33 : 107 - 112 .
32. Hesse S , Malezic M , Schaffrin A , Mauritz KH : Restoration of gait by combined treadmill training and multichannel electrical stimulation in non-ambulatory hemiparetic patients . Scand J Rehabil Med 1995 , 27 : 199 - 204 .
33. Hesse S , Bertelt C , Jahnke MT , Schaffrin A , Baake P , Malezic M , et al.: Treadmill training with partial body weight support compared with physiotherapy in nonambulatory hemiparetic patients . Stroke 1995 , 26 : 976 - 981 .
34. Hesse S , Konrad M , Uhlenbrock D : Treadmill walking with partial body weight support versus floor walking in hemiparetic subjects . Arch Phys Med Rehabil 1999 , 80 : 421 - 427 .
35. Lindquist AR , Prado CL , Barros RM , Mattioli R , da Costa PH , Salvini TF : Gait training combining partial body-weight support, a treadmill, and functional electrical stimulation: effects on poststroke gait . Phys Ther 2007 , 87 : 1144 - 1154 .
36. McCain KJ , Smith PS : Locomotor treadmill training with bodyweight support prior to over-ground gait: promoting symmetrical gait in a subject with acute stroke . Top Stroke Rehabil 2007 , 14 : 18 - 27 .
37. McCain KJ , Pollo FE , Baum BS , Coleman SC , Baker S , Smith PS : Locomotor treadmill training with partial body-weight support before overground gait in adults with acute stroke: a pilot study . Arch Phys Med Rehabil 2008 , 89 : 684 - 691 .
38. Patterson SL , Rodgers MM , Macko RF , Forrester LW : Effect of treadmill exercise training on spatial and temporal gait parameters in subjects with chronic stroke: a preliminary report . J Rehabil Res Dev 2008 , 45 : 221 - 228 .
39. Chen G , Patten C : Treadmill training with harness support: selection of parameters for individuals with poststroke hemiparesis . J Rehabil Res Dev 2006 , 43 : 485 - 498 .
40. Hidler J : Robotic-assessment of walking in individuals with gait disorders . Conf Proc IEEE Eng Med Biol Soc 2004 , 7 : 4829 - 4831 .
41. Alton F , Baldey L , Caplan S , Morrissey MC : A kinematic comparison of overground and treadmill walking . Clin Biomech (Bristol, Avon) 1998 , 13 : 434 - 440 .
42. Lee SJ , Hidler J : Biomechanics of overground vs. treadmill walking in healthy individuals . J Appl Physiol 2008 , 104 : 747 - 755 .
43. Parvataneni K , Ploeg L , Olney SJ , Brouwer B : Kinematic, kinetic and metabolic parameters of treadmill versus overground walking in healthy older adults . Clin Biomech (Bristol, Avon) 2009 , 24 : 95 - 100 .
44. Riley PO , Paolini G , Della CU , Paylo KW , Kerrigan DC : A kinematic and kinetic comparison of overground and treadmill walking in healthy subjects . Gait Posture 2007 , 26 : 17 - 24 .
45. Whittle M : Gait Analysis: An Introduction 4th edition . ButterworthHeinemann ; 2007 .
46. Daly JJ , Sng K , Roenigk K , Fredrickson E , Dohring M : Intra-limb coordination deficit in stroke survivors and response to treatment . Gait Posture 2007 , 25 : 412 - 418 .
47. Farmer SE , Pearce G , Stewart C : Developing a technique to measure intra-limb coordination in gait: applicable to children with cerebral palsy . Gait Posture 2008 , 28 : 217 - 221 .
48. Behrman AL , Lawless-Dixon AR , Davis SB , Bowden MG , Nair P , Phadke C , et al.: Locomotor training progression and outcomes after incomplete spinal cord injury . Phys Ther 2005 , 85 : 1356 - 1371 .