A. Biomechanical properties of the spastic ankle after stretching
Several studies have reported the positive effects of stretching subjects with ankle joint spasticity and/or contracture by improving soft-tissue extensibility, and decreasing muscle tone in stroke survivors [11,35,36]. Passive ankle stretching can be applied manually by physical therapists [13,37], external devices [14,38], and robotic systems [39,40]. Manual stretching by moving the spastic ankle through its ROM requires labor-intensive efforts. Furthermore, the outcome of manual stretching exercises is dependent on the experience of the therapist, and several clinical studies have shown insignificant improvements on ankle ROM after manual passive ankle stretching [14,37]. Thus, stretching boards [38] and robotic systems have served as alternative rehabilitation tools for stretching the ankles. Stretching boards have benefits (saving labor cost) and limitations (difficult to adjust the angle dynamically; inadequate security). The robot-aided rehabilitation of the ankle has been used effectively in treating ankle contracture and/or spasticity with the therapist able to help more patients at less cost and labor [41]. Previous studies indicated that this intervention reduced ankle joint resistance torque and stiffness, increased ROM [16], and improved balance and gait [36] in neurologically impaired patients. Robotic intervention in the form of intelligent stretching and active movement training has been studied in children with cerebral palsy and showed significant improvement in 12 children with CP in terms of improved passive and active ranges of motion, selective motor control, and mobility functions after 18 sessions of training [17]. Waldman [15] investigated the effects of the robotic rehabilitation of the ankle in stroke with ankle impairment, and the results showed patients in the robot group improved significantly more in dorsiflexion PROM, dorsiflexion strength, and balance and walking function, while the spasticity measured by the Modified Ashworth Scale was reduced more than that in the control group. Forrester [19] conducted similar studies, and the results suggested that robotic rehabilitation of the ankle was effective in improving balance and motor function poststroke.
In this study, to forcefully and safely stretch the ankle of a participant with spasticity to its extreme positions, we used an intelligent stretching device that stretched the joint with real-time feedback control of the resistance torque and stretching velocity. The stretching device was driven by a servomotor controlled by a digital signal processor [42], with the control algorithm described elsewhere [16]. By using this control strategy, the stretching device moved quickly in the middle (non-spastic) ROM and slowed down in the stiffer part of the ROM, while never exceeding preset stretching torques limits. This study demonstrated that improvement associated with the intelligent stretching of the spastic ankles post-stroke was consistent with previous research, and resulted in increased ROM and muscle strength, decreased ankle stiffness, and improved balance and mobility function. This type of high intensity, repetitive and efficient stretching can save demanding laborious work and be readily available to participants without the need of a skilled therapist. Furthermore, in this study, a significant correlation (τ=0.265, P=0.041) was observed between MAS and DF stiffness, which is consistent with the previous research [43]. This measure of stiffness may be used to obtain a more accurate and quantitative evaluation of biomechanical properties in the future.
B. Balance control
Postural stability, often defined as balance, plays an important role in the recovery of motor function in patients with hemiplegia. Three kinds of strategies are involved in postural control in humans: ankle strategy, hip strategy, and stride strategy [1,44]. The ankle strategy refers to the body’s center of gravity rotating or swinging around the ankle joint in a pendulum movement, which is the main strategy in normal people for maintaining balance when the support surface is firm and the perturbations are small [45,46]. The most important roles of the ankle joints are in controlling body sway and forward movements of the lower extremities, and these roles require the sophisticated passive (e.g. bones, ligaments) and active (e.g. muscles) anatomical structures, as well as by the interaction between these structures [47,48]. The ankle strategy is damaged partially after stroke creating muscular imbalance surrounding the ankle, increased joint stiffness, decreased proprioception of the ankle, and wrong central integration, which causes imbalance.
At present, various therapeutic methods have been used to improve balance post-stroke, such as task-related training assisted-robot walking, virtual reality rehabilitation, core strength exercises, visual feedback training, etc [49-52]. These methods of rehabilitation treat the patient as a whole, aiming to improve the posture control of the trunk and lower limbs. In our study, the application of robot-aided rehabilitation of the ankle is aimed at control of the ankle to improve balance function in stroke survivors. It forcefully, safely, and repeatedly stretched the ankle to its extreme positions resulting in structural changes in the viscoelastic properties of the connective tissues, thereby reducing ankle stiffness. The participants were asked to stare at the display screen where an amplified and lateral “ankle joint” image was shown as stretching the ankle from dorsiflexion to plantarflexion simultaneously. This kind of continuous visual feedback combined the correct depiction of proprioceptive and muscular motor sensation, which may ultimately lead to the reestablishment of ankle control. This process may produce various stimuli to the brain, to recover the damaged nervous system and coordination functions.
C. Pro-Kin balance test
Postural stability can be measured by assessing an individual postural sway through changes in the COP. The reliability of COP parameters, such as fluctuation, velocity, and area, to assess the postural control altered by stroke has been investigated [53]. This balance test system only requires participants to have a certain ability to sit or stand, and it can find subtle balance differences more comprehensively, making up for the measurement errors caused by subjective factors in the balance scales assessment.
In this study, the Pro-Kin was used to quantitatively evaluate the standing static balance of participants before and after training, excluding the influences of the hip strategy and stride strategy, and explore the role of ankle strategy in balance more accurately [33]. The results showed that, after the intelligent stretching training of the ankle joint, trajectory lengths, elliptical trajectory, L/M SD, F/B AS with closed eyes, and F/B SD with opened eyes decreased significantly, while the control group decreased significantly in trajectory length, and AS M/L with opened eyes, which confirmed that robot-aided rehabilitation of the ankle is of great significance in the implementation of ankle strategy. However, the balance scales failed to reflect the subtle differences in balance function after training between the two groups quantitatively.
Furthermore, we found that there were no significant improvements in trajectory lengths, elliptical trajectory, L/M SD, or L/M AS with opened eyes in the study group after training. As an explanation, we consider the following factors. Control of body balance relies on visual input, proprioception, and input from the vestibular system. The visual information may compensate for the loss of somatosensory function post-stroke and facilitate the human motor program in the brain. A previous study reported that the removal of the visual feedback aggrandized the COP sway [54]. So, stroke patients exhibited decreased postural stability during quiet stance under non-vision conditions, significant differences were easier to find with eyes closed but not open after training [55,56]. Furthermore, the intelligent stretching positively affected passive ankle stiffness in the sagittal plane (DF-PF), but not in the frontal plane. Previous studies reported that the weaker inter-limb coordination in AP direction after stroke may be on account of impaired balance control, while no significant differences were found in ML-COP fluctuation between two limbs of patients suggested the faint impact of hemiplegia on COP sway in ML direction [57], so there were no significant differences in COP sway in ML direction with opened eyes in the study group after training.
D. Correlations between DF stiffness and balance
In a quiet stance, several factors contribute to maintaining an upright position, including postural tone, background muscle tone with neural contributions, and the intrinsic stiffness of the muscle. The stroke survivors must rely on joint and muscle proprioceptors to minimize body movement or loss of balance [58,59]. There has been no study that quantitatively analyzed the impact of local biomechanical properties of the ankle on the overall balance function. This study further explored the correlation between ankle stiffness and the Pro-Kin balance test outcomes with opened eyes. The findings showed that the stiffness of dorsiflexion was positively related to trajectory length, elliptical trajectory, and average velocity M/L and F/B with opened eyes, and trajectory length was strongly positively related to the stiffness of dorsiflexion ( = 0.522, P =0.001), which meant that greater DF stiffness resulted in a worse balance function. But there was no significant correlation between PF stiffness and the Pro-Kin balance test outcomes, suggesting that DF stiffness was an important factor affecting the balance function, while PF stiffness was not, but the mechanism was not clear. We assumed that the decreased DF stiffness might activate the muscles around the ankles (especially the ankle dorsal flexor muscle) and increase the proprioceptive sense inputs and ROM of the ankle joint so that the ability to appropriately control balance during sway was improved through better coordination and mobilization of the senses and muscle functions of the ankle after intelligent stretching.
Study limitations
This study had some limitations. First, a small number of subjects were enrolled, further studies should increase the number of subjects to increase the power of the study. Second, no significant differences in biomechanical evaluations or Pro-Kin balance test outcomes between the two kinds of interventions were found. This might be because the training frequency, intensity, and total repetitions were not optimal. Third, the long-term effects of intelligent stretching training were unknown for a lack of a follow-up period. Further studies are necessary to address this issue. Our study only investigated the correlations between biomechanical properties and static balance in stroke survivors, the role of ankle function on dynamic balance require further investigation.