Changes in the temporal measures of swing phase duration also showed an improvement posttraining. Signals from the force-sensitive resistors were not available from S3 posttraining due to technical difficulties. There was a general trend for an increase in %swing on both the paretic and nonparetic side (Table 4), but this was not statistically significant (Z = −1.46, P = 0.14).
Because of the range in the number of training sessions that were completed by the participants, we examined whether there was a relationship between the 10MWT or mEFAP scores and the number of training sessions (Fig. 2). The duration of training (number of training sessions) was not significantly related to changes in the gait velocity (r = 0.52, P = 0.29), mEFAP scores (r = 0.32, P = 0.54), and no clear trends could be discerned. There was also no significant relationship between the Chedoke-McMaster foot or leg scores and functional ambulation outcomes, although there is a slight trend for participants with more physical impairment (ie, lower Chedoke-McMaster scores) to have greater percent improvement in functional ambulation (Fig. 2).
This study examined the effect of a treadmill-based locomotor training protocol using leg weights on functional ambulatory capacity. Although the sample size of this pilot study is small, the results indicate that treadmill-based locomotor training with leg weights is feasible and could be an effective strategy to improve functional ambulation in people with chronic stroke. Most participants showed an improvement in functional gait parameters, such as gait velocity and the ability to climb stairs, and an increase in the proportion of the step cycle spent in swing on the paretic side.
Treadmill-based locomotor training with partial body weight support has gained much attention as a promising approach to improve ambulation among people with incomplete spinal cord injury.42–46 However, there are mixed results about the efficacy of treadmill-based locomotor training in the chronic stroke population.47–49 The results of some clinical studies have suggested that strategies that provide a more challenging training environment, such as progressively increasing the treadmill speed50 or explicit practice of a variety of functional tasks,51,52 may be the key to producing functional improvements in ambulatory individuals after stroke. Although these reports have raised the issue of the clinical efficacy of treadmill-based locomotor training compared with other rehabilitation approaches, improved understanding of the neural and sensory control of walking is essential to ensure continued advances in gait rehabilitation strategies. We provided a more challenging training environment by affixing weights, scaled to body weight, around participants’ lower leg. The strategy of loading the flexor muscles by using leg weights was based on the concept that feedback during the swing phase can positively enhance ongoing flexor muscle activity, a finding that has been confirmed in both animal and human studies.26–29,53 Sensory feedback mediated by spinal reflex pathways from length- and load-sensitive afferents in flexor muscle have been shown to have an excitatory effect on ongoing flexor muscle activity in decerebrate cats.53,54 Rapid feedback-mediated facilitation of lower limb flexor muscles after mechanical swing phase perturbations has also been shown in adult humans.28,29,31,32 More recent studies have also shown that with repeated exposure to mechanical swing phase perturbations (eg, leg weights or resistance from robot-applied forces), humans develop anticipatory locomotor commands. Evidence for such anticipatory locomotor commands are revealed when the perturbation is unexpectedly removed and an aftereffect (eg, high stepping after swing phase resistance) is generated.26,29,30,33,55 Interestingly, one of our participants made a habit of walking around the laboratory at the end of each training session. He stated that he enjoyed the light feeling in his legs and that it seemed to be easier to walk after the weights were removed. In most participants, we observed that the proportion of the step cycle devoted to the swing phase increased toward normal expected values (40% of the step cycle),56,57 indicating that training with leg weights could have positively affected swing phase activity. The proportion of the step cycle devoted to the swing phase on the nonparetic limb also tended to increase but largely remained below normal expected values. Such minimal effects on nonparetic swing values (paretic limb stance) after treadmill-based locomotor training are consistent with previous reports.58
Recent evidence suggests that improvements in walking function posttraining could be attributed to changes in cortical drive during locomotion. Studies using transcranial magnetic stimulation or functional magnetic resonance imaging have indicated that there are increases in descending motor excitability and increases in the size of the cortical representation of lower limb muscles after single59 or repeated60–62 bouts of treadmill-based locomotor training in individuals with stroke. Enhanced cortical excitability and representation of the tibialis anterior muscle was also recently shown to be correlated to improved balance and step length following treadmill-based locomotor training.60 Improvements in functional ambulation were also shown to be associated with increased activation of cerebellar and midbrain areas after a six-month treadmill exercise program in individuals with chronic stroke.62 Considering that there is a particular contribution of cortical input to lower limb flexor muscles during walking,63–66 it is quite possible that changes in supraspinal input could have contributed to the changes in functional ambulation that we observed here after treadmill-based locomotor training with leg weights.
One previous study investigated the effect of leg weights in a small group (n = 3) of stroke survivors over a five-day training period.34 No significant effects on gait velocity were noted. In this study, participants underwent more intensive treadmill-based locomotor training with leg weights for a minimum of four weeks, three times per week. In addition, the amount of weight added to the legs was adjusted as a proportion of body weight and was based on previous findings about the relationship between added weight and level of flexor muscle activation during swing.30 However, we found no significant effects on overground gait velocity. Given that most of our participants’ initial gait velocity was in the range associated with the least-limited to full community ambulators,67 it may not be surprising that further improvements in gait velocity were not seen. Indeed, it was the participant who had the lowest initial gait velocity (S6) who showed the most marked improvements. In addition, we also note that four of our participants (S1, S3, S5, and S6) demonstrated a change in gait velocity of >0.10 m/sec. The standard error of measurement of the 10MWT has been reported to be 0.04 m/sec, and a change of 0.10 m/sec has been determined to be the threshold for determining substantial meaningful change in functional mobility.68
Although we did not observe significant improvements in overground gait velocity, other notable changes were observed, in particular, the improvements in stair climbing ability in most of the participants. Stair climbing is noted to be one of the most difficult mobility tasks among the poststroke69 and elderly70 population. Curiously, we did not observe a consistent improvement in the mEFAP subscore for obstacle crossing, another task that we expected would be particularly influenced by the hypothesized improvements in swing phase movement afforded by treadmill-based locomotor training with leg weights. Recent studies have described the gait characteristics of steps over obstacles in people with stroke.7,71 Reduced toe clearance and diminished knee flexion during the swing phase were suggested as contributing factors to the difficulties with obstacle clearance in people with stroke.7 However, the mEFAP subscore for obstacle avoidance is determined mainly by the time to completion. We did not conduct a kinematic analysis of obstacle crossing and therefore could have missed other qualities that might have improved, such as clearance height over the obstacles. Further studies are needed to determine whether the effects of this form of treadmill-based locomotor training with leg weights generalize to biomechanical improvements in gait characteristics during tasks such as obstacle crossing or stair climbing.
This was a pilot study that used a small sample of community-dwelling participants with mild stroke. Functional improvements in gait after treadmill-based locomotor training in these populations have been observed previously,48,49 so we cannot rule out the possibility that the positive effects that we observed could be attributable just to the training and not to a specific effect of the leg weights. Future studies stemming from this research are planned to include a larger sample of participants and the inclusion of a control intervention.
The amount of added weight around the leg was standardized at 5% of body weight. It is possible that this may not have provided enough of a training effect to significantly improve walking speed, stair climbing, or obstacle-crossing ability. Considering that many of our participants already had initial overground gait velocities more than 0.90 m/sec, modest improvements in this variable may not be surprising. Nevertheless, we still observed an overall mean improvement in gait velocity of 19% as well as promising results in the more difficult task of stair climbing, which improved in almost all participants. Further studies should determine whether this protocol may be improved by standardizing the amount of added weight according to the lower limb strength or ambulatory capacity rather than to body weight. This protocol was otherwise found to be safe and feasible with median Borg ratings of somewhat hard across all participants.
This pilot study demonstrates that treadmill-based locomotor training combined with leg weights could be a feasible approach for improving the ability to perform complex walking tasks, such as stair climbing, in individuals with chronic stroke. Further work must be conducted to differentiate the specific benefit of adding leg weights versus the effect of treadmill-based locomotor training alone.
The authors thank A. Burke, B. Cowie, F. Lam, S. Liu, S. Hua, J. Shcherbakova, and T.D. Wingson for their valuable assistance and to all the participants who took part in this study. Tania Lam is a Canadian Institutes of Health Research New Investigator.
1. Barbeau H, Fung J. The role of rehabilitation in the recovery of walking in the neurological population. Curr Opin Neurol.
2. Visintin M, Barbeau H, Korner-Bitensky N, et al. A new approach to retrain gait in stroke patients through body weight support and treadmill stimulation. Stroke.
3. Harkema SJ, Hurley SL, Patel UK, et al. Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol.
4. Duysens J, Clarac F, Cruse H. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev.
5. Olney SJ, Richards C. Hemiparetic gait following stroke. I. Characteristics. Gait Posture.
6. Hartman-Maeir A, Soroker N, Ring H, et al. Activities, participation and satisfaction one-year post stroke. Disabil Rehabil.
7. Said CM, Goldie PA, Culham E, et al. Control of lead and trail limbs during obstacle crossing following stroke. Phys Ther.
8. Said CM, Goldie PA, Patla AE, et al. Obstacle crossing in subjects with stroke. Arch Phys Med Rehabil.
9. Lehmann JF, Condon SM, Price R, et al. Gait abnormalities in hemiplegia: Their correction by ankle-foot orthoses. Arch Phys Med Rehabil.
10. Lehmann JF, Esselman PC, Ko MJ, et al. Plastic ankle-foot orthoses: Evaluation of function. Arch Phys Med Rehabil.
11. Wieler M, Stein RB, Ladouceur M, et al. Multicenter evaluation of electrical stimulation systems for walking. Arch Phys Med Rehabil.
12. Liberson WT, Holmquest HJ, Scot D, et al. Functional electrotherapy: Stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. Arch Phys Med Rehabil.
13. Granat MH, Maxwell DJ, Ferguson AC, et al. Peroneal stimulator; evaluation for the correction of spastic drop foot in hemiplegia. Arch Phys Med Rehabil.
14. Burridge JH, Taylor PN, Hagan SA, et al. The effects of common peroneal stimulation on the effort and speed of walking: A randomized controlled trial with chronic hemiplegic patients. Clin Rehabil.
15. Kottink AI, Oostendorp LJ, Buurke JH, et al. The orthotic effect of functional electrical stimulation on the improvement of walking in stroke patients with a dropped foot: A systematic review. Artif Organs.
16. Lindquist AR, Prado CL, Barros RM, et al. Gait training combining partial body-weight support, a treadmill, and functional electrical stimulation: Effects on poststroke gait. Phys Ther.
17. 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.
18. 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.
19. 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.
20. Yan T, Hui-Chan CW, Li LS. Functional electrical stimulation improves motor recovery of the lower extremity and walking ability of subjects with first acute stroke: A randomized placebo-controlled trial. Stroke.
21. Daly JJ, Roenigk KL, Butler KM, et al. Response of sagittal plane gait kinematics to weight-supported treadmill training and functional neuromuscular stimulation following stroke. J Rehabil Res Dev.
22. Brissot R, Gallien P, Le Bot MP, et al. Clinical experience with functional electrical stimulation-assisted gait with Parastep in spinal cord-injured patients. Spine.
23. Gallien P, Brissot R, Eyssette M, et al. Restoration of gait by functional electrical stimulation for spinal cord injured patients. Paraplegia.
24. Granat MH, Heller BW, Nicol DJ, et al. Improving limb flexion in FES gait using the flexion withdrawal response for the spinal cord injured person. J Biomed Eng.
25. Nicol DJ, Granat MH, Tuson SJ, et al. Variability of the dishabituation of flexion reflexes for FES assisted gait in spinal injured man. Med Eng Phys.
26. Lam T, Wolstenholme C, Yang JF. How do infants adapt to loading of the limb during the swing phase of stepping? J Neurophysiol.
27. Garrett M, Luckwill RG. Role of reflex responses of knee musculature during the swing phase of walking in man. Eur J Appl Physiol Occup Physiol.
28. Ghori GM, Luckwill RG. Pattern of reflex responses in lower limb muscles to a resistance in walking man. Eur J Appl Physiol Occup Physiol.
29. Lam T, Anderschitz M, Dietz V. Contribution of feedback and feedforward strategies to locomotor adaptations. J Neurophysiol.
30. Lam T, Wirz M, Lunenburger L, et al. Swing phase resistance enhances flexor muscle activity during treadmill locomotion in incomplete spinal cord injury. Neurorehabil Neural Repair.
31. Dietz V, Quintern J, Boos G, et al. Obstruction of the swing phase during gait: Phase-dependent bilateral leg muscle coordination. Brain Res.
32. Ghori GM, Luckwill RG. Phase-dependent responses in locomotor muscles of walking man. J Biomed Eng.
33. Noble JW, Prentice SD. Adaptation to unilateral change in lower limb mechanical properties during human walking. Exp Brain Res.
34. Kollen BJ, Rietberg MB, Kwakkel G, et al. Effects of overloading of the lower hemiparetic extremity on walking speed in chronic stroke patients: a pilot study. NeuroRehabilitation.
35. Sharp SA, Brouwer BJ. Isokinetic strength training of the hemiparetic knee: effects on function and spasticity. Arch Phys Med Rehabil.
36. Weiss A, Suzuki T, Bean J, et al. High intensity strength training improves strength and functional performance after stroke. Am J Phys Med Rehabil.
37. Gowland C, Stratford P, Ward M, et al. Measuring physical impairment and disability with the Chedoke-McMaster Stroke Assessment. Stroke.
38. Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc.
39. Baer HR, Wolf SL. Modified emory functional ambulation profile: an outcome measure for the rehabilitation of poststroke gait dysfunction. Stroke.
40. Liaw LJ, Hsieh CL, Lo SK, et al. Psychometric properties of the modified Emory Functional Ambulation Profile in stroke patients. Clin Rehabil.
41. Pett MA. Nonparametric Statistics for Health Care Research.
Thousand Oaks, CA: Sage Publications; 1997.
42. Behrman AL, Lawless-Dixon AR, Davis SB, et al. Locomotor training progression and outcomes after incomplete spinal cord injury. Phys Ther.
43. Hornby TG, Zemon DH, Campbell D. Robotic-assisted, body-weight-supported treadmill training in individuals following motor incomplete spinal cord injury. Phys Ther.
44. Wernig A, Nanassy A, Muller S. Maintenance of locomotor abilities following Laufband (treadmill) therapy in para- and tetraplegic persons: follow-up studies. Spinal Cord.
45. Wirz M, Zemon DH, Rupp R, et al. Effectiveness of automated locomotor training in patients with chronic incomplete spinal cord injury: a multicenter trial. Arch Phys Med Rehabil.
46. Wernig A, Muller S, Nanassy A, et al. Laufband therapy based on ‘rules of spinal locomotion’ is effective in spinal cord injured persons. Eur J Neurosci.
47. Liston R, Mickelborough J, Harris B, et al. Conventional physiotherapy and treadmill re-training for higher-level gait disorders in cerebrovascular disease. Age Ageing.
48. Ada L, Dean CM, Hall JM, et al. A treadmill and overground walking program improves walking in persons residing in the community after stroke: a placebo-controlled, randomized trial. Arch Phys Med Rehabil.
49. Macko RF, Ivey FM, Forrester LW, et al. Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke: a randomized, controlled trial. Stroke.
50. Pohl M, Mehrholz J, Ritschel C, et al. Speed-dependent treadmill training in ambulatory hemiparetic stroke patients: a randomized controlled trial. Stroke.
51. Dean CM, Richards CL, Malouin F. Task-related circuit training improves performance of locomotor tasks in chronic stroke: a randomized, controlled pilot trial. Arch Phys Med Rehabil.
52. Bassile CC, Dean C, Boden-Albala B, et al. Obstacle training programme for individuals post stroke: feasibility study. Clin Rehabil.
53. Lam T, Pearson KG. Proprioceptive modulation of hip flexor activity during the swing phase of locomotion in decerebrate cats. J Neurophysiol.
54. Lam T, Pearson KG. Sartorius muscle afferents influence the amplitude and timing of flexor activity in walking decerebrate cats. Exp Brain Res.
55. Emken JL, Reinkensmeyer DJ. Robot-enhanced motor learning: accelerating internal model formation during locomotion by transient dynamic amplification. IEEE Trans Neural Syst Rehabil Eng.
56. Dubo HI, Peat M, Winter DA, et al. Electromyographic temporal analysis of gait: normal human locomotion. Arch Phys Med Rehabil.
57. Peat M, Dubo HI, Winter DA, et al. Electromyographic temporal analysis of gait: hemiplegic locomotion. Arch Phys Med Rehabil.
58. Patterson S, Rodgers MM, Macko RF, et al. Effect of treadmill exercise training on spatial and temporal gait parameters in subjects with chronic stroke: a preliminary report. J Rehabil Res Dev.
59. Forrester LW, Hanley DF, Macko RF. Effects of treadmill exercise on transcranial magnetic stimulation-induced excitability to quadriceps after stroke. Arch Phys Med Rehabil.
60. Yen CL, Wang RY, Liao KK, et al. Gait training induced change in corticomotor excitability in patients with chronic stroke. Neurorehabil Neural Repair.
61. Dobkin BH, Firestine A, West M, et al. Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. Neuroimage.
62. Luft AR, Macko RF, Forrester LW, et al. Treadmill exercise activates subcortical neural networks and improves walking after stroke: A randomized controlled trial. Stroke.
63. Bonnard M, Camus M, Coyle T, et al. Task-induced modulation of motor evoked potentials in upper-leg muscles during human gait: A TMS study. Eur J Neurosci.
64. Capaday C, Lavoie BA, Barbeau H, et al. Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol.
65. Petersen NT, Butler JE, Marchand-Pauvert V, et al. Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking. J Physiol (London
66. Schubert M, Curt A, Jensen L, et al. Corticospinal input in human gait: Modulation of magnetically evoked motor responses. Exp Brain Res.
67. Perry J, Garrett M, Gronley JK, et al. Classification of walking handicap in the stroke population. Stroke.
68. Perera S, Mody SH, Woodman RC, et al. Meaningful change and responsiveness in common physical performance measures in older adults. J Am Geriatr Soc.
69. Stineman MG, Fiedler RC, Granger CV, et al. Functional task benchmarks for stroke rehabilitation. Arch Phys Med Rehabil.
70. Williamson JD, Fried LP. Characterization of older adults who attribute functional decrements to “old age.” J Am Geriatr Soc.
71. Den Otter AR, Geurts AC, de Haart M, et al. Step characteristics during obstacle avoidance in hemiplegic stroke. Exp Brain Res.