The findings of this study suggest that AMT-EST has several key advantages for proprioception of ankle EV, PROM of ankle INV and EV, and strength of ankle DF, INV, and EV compared with general ES (p < 0.05). In addition, FM-L showed a significant improvement in the experimental group on between-group comparison, and the other functional abilities, including balance and gait, significantly increased in the AMT-EST group from the baseline to after the intervention.
To restore sensorimotor function and functional abilities in stroke patients, ES has been used commonly in the clinical setting. Recently, the effect of ES combined with functional motion has been reported to further enhance afferent inputs to promote motor performance [23]. For example, the application of ES on ankle muscles during gait and everyday activities significantly increased ankle proprioception and ankle strength, balance, and gait speed [24]. However, such a performance includes complex movement of the entire lower extremity. Because ankle impairment is more prominent and voluntary ankle motor control is more difficult than the movement of other lower extremities in stroke patients, a focus on ankle training with ES while excluding other lower extremity movement is required. In this study, the application of ES to the ankle dorsiflexor (tibialis anterior) and evertor (peroneus longus) along with functional ankle training was associated with significant improvements in ankle PROM and strength, as well as in the ankle proprioception. When ES is applied with a focus on ankle function movement, it can enhance the generation of cortical brain perfusion to the ipsilesional sensorimotor cortex for restoring ankle sensorimotor function [25]. Furthermore, the repeated ankle movement training provides sensory input for muscle extensibility, which is responsible for the stretch receptors of the muscle spindle. Moreover, ankle movement training is effective in promoting ankle proprioception that recognizes the positional sense of joints with respect to changes in muscle length [26]. By contrast, the control group received ES without the ankle movement training to the same ankle dorsiflexor and evertor, which are generally stimulated electrically in a clinical environment. After the completion of a 20-session training, the balance ability of the control group, including BBS and TUG, was improved (p < 0.05); however, there was no significant improvement of the ankle function. The participants of this study were all chronic stroke patients, with a post-stroke duration of 10.5 months, and general physical therapy, such as gait training, was performed equally for all participants. These results demonstrate that AMT-EST is more effective than conventional ES training for ankle function in hemiparetic stroke patients. Therefore, it can be postulated that additional concentrated ankle training, such as AMT-EST, is required to improve ankle function in chronic stroke patients.
The passive biaxial ankle movement used in this study is characterized by reproducing the ankle subtalar joint movement (INV-EV) to a single axis movement (DF-PF). After training, the results showed significant improvement in the ankle proprioception, PROM, and strength, particularly on ankle INV and EV. There was a significant improvement in balance and gait function. This implies the importance of the roles of the ankle invertors and evertors that constitute the muscles of the medial and lateral sides of the ankle. The peroneus longus and brevis muscles, which are the primary ankle evertors, pass lateral to the subtalar joint, and their primary function is foot pronation and weak PF. Similarly, the tibialis anterior and posterior muscles are the primary ankle invertors and pass medial to the subtalar axis and cause ankle DF and PF, respectively. Depending on the muscle attachment site (origin and insertion), these muscles complement each other in an INV and EV, as well as in the overall ankle movement. These results may suggest that ankle proprioception and PROM enhancement of the primary invertor and evertor would have affected the power of voluntary muscle contraction of not only the ankle invertor and evertor but also ankle dorsiflexor and functional performances.
Sensory information from the ankle has been demonstrated to be associated with the perception of verticality [27], which in turn is related to balance [28]. More importantly, because the planning and execution of voluntary movement requires sensory information on body position and the prediction of future position, activities such as balancing can be difficult with severe impairment of ankle sensation. Therefore, the impaired ankle sensory function is considered important in the recovery of physical function in stroke patients. Recent studies have found that ankle proprioceptive deficits have significant relationships with mobility, balance, balance confidence, physical functions, and activities of daily living [29, 30]. The results of this study showed that ankle proprioception had a moderate correlation with PROM, strength, BBS, and FM-L. Furthermore, the significant improvements in ankle proprioception and improved FM-L, BBS, and TUG in this study support the earlier evidence. Nonetheless, the role of sensory function in complex performance is somewhat different from that of balance. The performance of complex functions, such as walking, involves various factors including muscle strength [31–33], spasticity [32], cognition [34], motor function [33, 34], and balance [31, 33], as well as sensory information. A recent meta-analysis showed that leg somatosensory retraining after stroke significantly improved the somatosensory function and balance but not the gait [35]. However, this meta-analysis included only a few ankle proprioception-related training, and a 2-week proprioception training of the big toe and ankle was reported to be effective for improving light touch, postural control, and gait but not proprioception [36]. This study performed perception training consisting only of reposition training of the foot and ankle. Therefore, the evidence for effective proprioception training methods and their effect on functional ability is still insufficient. Nevertheless, it is clear that sensory impairments play an important role in motor recovery and physical function in stroke patients. Depending on the lesion location, strokes can damage both the motor and sensory neural systems, block the closed loop between the brain and body, and thus lead to neurological impairment that is associated with significant physical dysfunction [37, 38]. Further studies on brain plasticity for sensory function recovery in brain lesions should be considered.
Individuals with proprioception deficits experience low balance confidence as well as impaired balance and lack of independence in daily living [29]. Balance confidence, which is significantly correlated with balance (BBS, r = 0.44) and mobility (TUG, r = -0.43) of stroke patients [39], is closely related to fall efficacy. This study did not show a significant correlation between ankle proprioception and fall efficacy, but showed a significant improvement in fall efficacy after AMT-EST. Moreover, the participants in the experimental group reported a markedly positive improvement in confidence than those in the control group. We believe that AMT-EST of paretic ankle promotes psychological factors that are related to balance confidence as well as balance ability, and related research should be conducted.
To our knowledge, this is the first randomized controlled trial that applied intensive passive biaxial ankle movements with ES for improving ankle sensorimotor function. The novelty of this study is that the ankle training and proprioceptive measurements in this study were performed in the biaxial ankle direction and at a subdivided angle. Nonetheless, this study has several limitations. First, the small sample size, insufficient intervention intensity, and intervention period detract from the strength of the findings. Second, the long-term effects of the training could not be confirmed. Third, we could not exclude a learning effect for each evaluation system. Finally, ankle motor control and ankle muscle activity could not be directly determined. Future studies need to study the optimal intensity and duration of this ankle intervention for stroke patients with ankle sensorimotor impairment. Therefore, it is difficult to generalize the effect of ankle training to stroke patients in with the results of this study. The evidence of brain plasticity for sensory recovery should be investigated.