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. [
13] 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 [
39].
Regardless of the approach, BWSLT leads to improvements in gait quality. This conclusion is in accordance with a recent review of Merholz et al. [
17] 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 [
40].
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. [
14] 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 Field-Fote et al. [
14], 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 [
41], 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 [
14], 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 [
45]. 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 [
7].
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.
Limitations
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 neuropathology.
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 [
6]. It is also possible that a combination of treadmill-based BSWLT and overground training without body weight support may be the optimal approach [
48]. However, direct comparisons must be made in individuals with chronic SCI before definitive conclusions can be reached.