Evaluating the effects of delivering integrated kinesthetic and tactile cues to individuals with unilateral hemiparetic stroke during overground walking

To determine the effects of the proposed integrated cue system an experimental setup of overground walking was arranged. Ten individuals with hemiparetic stroke took part in the trials. Participants of the study had suffered single onset of unilateral hemiparetic stroke, and were in the sub-acute phase of recovery, were able to walk 10 m without assistance and had a 3 or higher Brunnstrom stage [56]. Individuals who were unable to follow verbal request, or had foot drop condition, limitations in joint range of motion, pain in the lower extremities, unstable medical conditions, or other diagnosed neurologic or musculoskeletal diseases were excluded from the study. Demographic details (mean ± standard deviation (SD) or counts) of the participants are presented in Table 1. All participants were inpatients of the Rehabilitation Center of Gyeongsang National University Hospital (Jinju, Republic of Korea). Gait training, strengthening and endurance exercise, and balance training were applied to the patients in their current rehabilitation program. All recruited subjects gave written informed consent approved by our local Ethics Committee before participating in the study.

Each subject was first introduced to the system and its functionality. The patient grasps the handle of HCD to switch on its operation. HCD allows the patient to receive kinesthetic cue and walk within a range of gait speeds set by the operator. Meanwhile VFD provides a tactile cue on the paretic shank during swing phase. Subject wears a waist mounted leather belt holding a smartphone for evaluation of trunk sway and wireless electromyography (EMG) sensors (Wireless EMG Probes by NORAXON USA) [57] to monitor muscle activity. Recently, we utilized smartphone as a reliable tool to assess body sway parameters [48], [58, 59]. The smartphone ran a custom-made android application that identified trunk tilt and provided this information to a socket program on the operator’s computer at 100 Hz. EMG data was recorded at 1.5 kHz, for four muscles each of the paretic and healthy legs (vastus medialis obliquus (VMO), semitendinosus (SMT), tibialis anterior (TBA) and gastrocnemius medialis (GCM)). Stance times of healthy and paretic leg calculated by the Arduino Due on the VFD were sent to a custom-built MATLAB GUI through XBee. All subjects walked 10 m distance in each trial; data obtained during the middle 6.5 m was recorded for analysis. A 10 m walk can give an adequate representation of the post-stroke walking ability [60]. The scheme of administering haptic cues used in this study was adopted to assess their individual and combined effects on gait parameters. Furthermore, the speed of HCD was selected to achieve an increase of up to 40% in the user’s preferred gait speed. As, various exercise therapy regimes have been found to achieve up to 40% increase in initial gait speeds [61]. Each trial condition was performed two times by the participants and the mean was analyzed. Four cue combinations and three gait speeds were tested per participant. The cue combinations were No Cue walk (NCW), Tactile Cue walk (TCW), Kinesthetic Cue Walk (KCW), and Integrated Cue Walk (ICW). The speed settings were 0% (+ 0%), 20% (+ 20%), and 40% (+ 40%) increases in the subject’s normal gait speed. The details of the trial conditions are described in Table 2. All participants wore comfortable walking shoes with removable insoles to accommodate the custom-made insoles of the VFD. A physical therapist walked beside the subject during the walking trials. Participants were given a break of 1 min in between trials.

During each walking trial, various parameters were recorded for post-experimental data analysis. Figure 2 illustrates the communication interface of the various devices used in this research. HCD was operated over Wi-Fi with a personal computer running a custom-built LabVIEW GUI program. This GUI commanded the HCD to setup various walking speeds during trials. It also handled the smartphone communication over Wi-Fi and saved the body sway data for post-experimental analysis. Later we calculated RMS of Mediolateral (ML) tilt to determine the condition of balance during various walking trials. The tilt in Mediolateral plane (ML tilt) is the sideways sway a human body experiences while maintaining an upright stance or walking. The RMS of ML Tilt has been utilized as a reliable marker of postural control during walking [62, 63]. Stance times received from the VFD were stored on the personal computer and utilized to define Stance Symmetry Ratio (i.e., Stance Symmetry Ratio (SSR) = stance time of healthy side / stance time of paretic side). The use of wireless EMG Sensors minimized the noise and artifacts of electrical and mechanical origins. The recorded EMG signals were band pass filtered (20–400 Hz), rectified, and smoothed with RMS filter at 100 ms [64]. To identify the increase in muscle activity of paretic side percentage of non-paretic peak activity (%NPA) was calculated, where integrals of EMG values of the paretic muscles during stance and swing phase were normalized to the EMG integrals from peak activity of the same muscles on the non-paretic side [30, 65, 66].

A one-way repeated measures analysis of variance (ANOVA) was performed to study the effects of Cue (factor), at preferred gait speed, which had four levels (no cue (NCW), tactile cue (TCW), kinesthetic cue (KCW + 0%) and integrated cue (ICW + 0%)) on RMS of ML Tilt, Stance Symmetry Ratio and %NPA in the four paretic muscles. Moreover, a two-way repeated measures ANOVA was used to identify the effects of Haptic Cue (factor, levels: kinesthetic (KCW) and integrated (ICW)) and increase in Gait Speed (factor, levels: 0%, 20% and 40%) on RMS of ML Tilt, Stance Symmetry Ratio and %NPA in the four paretic muscles. In addition, Mauchly’s test of Sphericity was used and Greenhouse-Geisser corrections were applied in case of its violation. Post hoc tests were conducted using the Bonferroni correction method. Partial eta squared (η²) was calculated as a measure of the effect size for one- and two-way repeated measure analysis of variance; Cohen’s d was also calculated and used for pairwise comparisons. All statistical analysis was performed using SPSS V20.0 (IBM Corp., Armonk, NY, USA).

The HCD allows the users to only apply limited load on the upper limb and encourages them to involve their paretic lower limb in order to achieve increase in muscle activity. In the No Cue Walk (NCW) and Tactile Cue Walk (TCW) trials, the participants possibly used compensatory and adaptive mechanisms of the nonparetic leg and trunk in motor control, where they coped with existing deficits including biomechanical changes rather than by regaining the appropriate sequence of muscle activation [67]. Whereas, with the introduction of the HCD in Kinesthetic Cue Walk (KCW) and Integrated Cue Walk (ICW) trials, the users tend to engage their paretic lower limb muscles more actively. Similar to our results, using an instrumented cane for restricted loading of upper limb led to increase in EMG of paretic leg muscles [30]. Vastus medialis obliquus (VMO) and semitendinosus (SMT) are the muscles vital in maintaining the upright body posture during stance phase of gait [32]. Thus, increased activation of these muscles at preferred gait speed also contributed to postural control during walking. Motor training to induce the use of the affected side increases activity in the lesioned hemisphere [68]. Therefore, the provision of a kinesthetic cue may facilitate the post-stroke gait rehabilitation by increasing paretic muscle activity.

Stroke disrupts the ability to maintain posture and equilibrium during walking [69]. With the use of HCD subjects may increase their base of support, thus allowing a greater range of center of mass motion while maintaining stability. Subject’s contact with the HCD also provides proprioceptive augmentation, which is beneficial in improving postural stability [30, 70]. Therefore, the contribution of kinesthetic cues from the hand to postural control suggests that the HCD may be useful not only in creating biomechanical advantages; but also in providing additional spatial orientation information for control of balance during overground walking. This is evident from the results obtained where the trunk sway (RMS of ML Tilt) of participants was better, albeit not statistically significantly so, during trials with HCD (KCW and ICW), as compared to those without it (NCW and TCW).

Hemiparesis is the most common impairment among the subjects who suffer a stroke, which can result in asymmetry of gait. In post-stroke gait, increase of the vertical ground reaction forces through the healthy limb is positively correlated with temporal asymmetry [71]. Therefore, musculoskeletal health of the non-paretic limb is also negatively affected by an asymmetric post-stroke gait. Stance symmetry ratio (SSR) is correlated with swing time and step length symmetry ratio, thus it can indicate improvements in gait symmetry [72]. A stance ratio of 1 is desired for normal/healthy walking condition [73]. Application of external cues using vibratory stimulation during gait may control gait parameters and improve gait performance in chronic stroke patients [34]. The afferent signals due to vibration increase the excitability of several segments of the spinal cord and could facilitate triggering of locomotor-like movements [74, 75]. High-frequency low-amplitude mechanical vibrations, applied to a muscle-tendon unit, generate afferent fiber discharges because of the activation of muscle spindles [74]. The modulation of afferent inputs alters the excitability of the corticospinal pathway [75] as well as the activation of cortical motor regions [76]. During low-amplitude biceps muscle tendon vibration, most of the functionally linked primary motor cortex cells respond mainly with excitatory firing [76]. At preferred gait speed during TCW trials, tactile cue induced substantial improvements in stance symmetry (as expected). This result may be due to increase of somatosensory afferent signals. Similarly, step-synchronized vibration stimulation of the soles improved gait steadiness in Parkinson’s disease patients with predominantly balance impairment, presumably by enhancing sensory feedback [77]. Proprioceptive afferents can play a key role in calibrating the spatial motor frame of reference and provide a powerful sensory augmentation to the central nervous system [78]. Moreover, gait speed and balance (Table 3) were not disturbed by provision of the tactile cues. Tactile cue is a constant vibration during swing phase to reduce the spasticity and improve the smoothness of motion in lower extremity during gait cycle, hence contributing towards improvement of gait symmetry. Temporal asymmetry is correlated with motor recovery [79]. Therefore, the provision of a tactile cue may facilitate post-stroke gait rehabilitation by improving the temporal stance symmetry.

The trunk sway of participants during walking as seen from the RMS of ML Tilt (Table 3) was similar in KCW + 0% and ICW + 0% but was better (not statistically significant) as compared to NCW trial. Increase in percentage of non-paretic peak activity (%NPA) of paretic muscles, VMO and SMT, was evident and alike in KCW + 0% and ICW + 0% as compared to NCW trial. Likewise, similar improvements of SSR in TCW and ICW + 0% trials were observed as compared to NCW trial. Thus at preferred gait speed, subjects tend to walk with increased symmetry and muscle activity due to the combined effects of HCD and VFD assimilating without disruption in balance.

Gait speed is considered to be an important marker of deficit severity and functional ability after stroke [80]. Thus, speed gains resulting from the application of HCD’s kinesthetic cue may become the object of considerable interest in future clinical studies on gait rehabilitation. Post-stroke gait at increased speeds may allow more appropriate timing of lower limb muscles, improved movement coordination, and possibly facilitation of intra-limb and inter-limb energy transfers [81]. Therefore, the increase in muscle activity at higher gait speeds could be beneficial for post-stroke gait training. No statistically significant difference according to Haptic Cues in %NPA of paretic muscles existed as HCD was utilized in both conditions (ICW and KCW). On the other hand statistically significant difference in %NPA of paretic muscles, VMO and SMT, according to gait speed was observed, mainly attributed to the increase in gait speed.

We observed that participants could comfortably increase their gait speed while utilizing the proprioceptive augmentation through HCD. This proprioceptive augmentation aided the subjects in balance control during walking in KCW and ICW trials. No statistically significant difference at various walking speeds in RMS of ML tilt and no statistically significant difference according to Haptic Cues in RMS of ML tilt existed, as these trials included use of HCD.

Statistically significant improvement in SSR observed between KCW and ICW at 0% increased gait speed is attributed to the involvement of tactile cue. Whereas, no statistically significant difference in SSR at increased gait speeds (+ 20% and + 40%) was observed between KCW and ICW. This may be due to the increased influence of gait speed on temporal asymmetry as compared to that of tactile cue. As, post-stroke ambulatory subjects who are severely asymmetric appear more likely to exhibit improved temporal symmetry at their faster walking speeds [40]. For both ICW and KCW trials, increase in gait speed from 0% to 20% exhibited improvements in SSR and further increase of gait speed to 40% worsened it. This may be attributed to the limitations of hemiparetic gait. Level of gait functionality in post-stroke ambulatory subject limits the potential to increase the walking speed and introduces the need for compensations on the non-paretic side [82].

The suggested integrated cue system comprises of two independent devices (HCD and VFD) operated through a personal computer; however, for a patient self-usable system certain possible modifications are necessary which include the fusion of HCD and VFD into a single device, and making the device operable (data collection and monitoring) with a smartphone. The improvements in gait parameters, as observed during the use of integrated cues by the participants, including stance symmetry ratio and percentage of non-paretic peak activity will benefit the sub-acute unilateral hemiparetic stroke suffering individuals to overcome gait deficiencies. Nevertheless, it is essential to observe the translation of these improvements in clinical measures of gait rehabilitation (Functional Gait Assessment, 6 Minute Walk Test, Dynamic Gait Index, Timed Up and Go, etc.) following a gait training study using the proposed system. Observations with a small group of participants is a limitation of this study; thus further studies are necessary to explore the effects of the proposed system in detail with greater diversity of participants and grouping them into categories of different functional abilities and gait speeds. The future continuation of this research will include evaluation of the level of persistent gait improvement and long-term performance retention in participants. The eventual goal of this research is to devise a system that can be used in non-laboratory settings for gait rehabilitation of individuals with sub-acute stroke.