A clinically meaningful improvement of the upper limb motor function was consistently revealed in all motor measures after the experimental intervention, but not after conventional physical therapy. Similar limited effects were detected in the sensory function in both groups.
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The combined tDCS and VR-based paradigm provided not only greater but also clinically meaningful improvement in the motor function (and similar sensory effects) in comparison to conventional physical therapy.
Non-invasive brain stimulation, such as transcranial magnetic stimulation and transcranial direct current stimulation (tDCS) have been proved to modulate cortical excitability through the application of a magnetic field or low-intensity electric current to the scalp using a coil or saline-soaked electrodes, respectively. When applied to the primary motor cortex, it may prime neuroplasticity and motor learning effects [28], which have been shown to improve motor function after stroke [29, 30]. While current evidence suggests a similar potential effectiveness of both techniques [31, 32], the overall lower costs, lower safety risks, and potential to be applied concurrently during rehabilitation of tDCS can facilitate its clinical integration [33]. In contrast to the inconsistent results in its earlier stages, tDCS has shown positive results at improving motor function of the paretic upper limb in chronic stroke [34, 35]. Interestingly, the combination of tDCS and mirror therapy has shown additive effects on motor performance [36] and, similarly, its combination with motor imagery has been reported to modulate not only the neural correlates of movement [37,38,39], but also the motor performance of upper limb tasks [40, 41].
This study was registered at clinicaltrials.gov (NCT03528018; Retrospectively registered on May 17, 2018) and was approved by the Institutional Review Board of Hospital Vithas Valencia al Mar. All subjects who satisfied the inclusion criteria and accepted the terms of participation in the study provided informed written consent before enrollment.
It is also important to highlight that four individuals out of the 14 participants in the experimental group (28.6%) did not show any motor improvement. This effect was indicated by inexistent (no change) or scant (one-point change) improvements using the Fugl-Meyer Assessment Scale, and was confirmed by an absence of improvements using the subscales of the Wolf Motor Function Test. No clinical or demographic differences were found between these participants and the remaining participants of the experimental group.
This study investigated the effectiveness of a combined tDCS and VR-based intervention on upper limb function in chronic individuals post-stroke with persistent severe hemiparesis in comparison to a conventional physical therapy intervention. Our results provide evidence that participation in self-triggered motor observation tasks, coupled with tDCS, can provide clinically meaningful improvements in the motor function when compared to conventional physical therapy alone, while having similar effects on the sensory function.
Improvement in the motor function detected in the body structure, evidenced by the Fugl-Meyer Assessment Scale, is supported by similar interventions combining tDCS and VR in individuals with acute stroke and mild impairment, with changes of up to 10 points on the same scale reported [77, 78]. Although the amelioration experienced by the participants was less dramatic, the relevance of their progress should be highlighted due to their time since injury and the severity of their impairment, as both attributes have been reported to limit the expected benefits of post-stroke interventions [9, 79]. Improvements detected in the body activities, evidenced by the Wolf Motor Function Test, are consistent with the results from the body structure. The enhancement of both performance time and functional ability are not only supported by previous reports, but also exceeded the reported benefits obtained by mildly impaired individuals in the acute phase post-stroke [78]. However, interpretation of the results in this scale should be done with caution considering the small effect size detected in our study. Although the remarkable progress of the participants in our study could be explained by their greater room for improvement, as they presented severely impaired function, it should be taken into account that the severity of the motor function is also the worst prognostic factor for upper limb functional recovery [9]. The improvement detected in the motor function after the experimental intervention might have a particular clinical relevance for the treatment of individuals with the most chronic and severe hemiparesis, as the detected changes were not only statistically significant, but also were clinically meaningful. Importantly, although statistical significance is required to validate any treatment effect, the clinical relevance of the statistical findings is often arguable and, in some cases, very limited [80]. The overcoming of the minimal clinically important difference of both measures of motor function after the experimental intervention support that the improvements in this ability could be effectively perceived by the participants and mandate a change in their clinical management. The detected changes, translated into the clinic, meant that some individuals who were not able to perform hand, wrist, or multi-joint movements and had no movement from single joint extensor and flexor muscle synergies before the experimental intervention, showed certain capacity, although being very limited, to perform these movements after the intervention. The general improvement in motor function after the combined intervention of tDCS and VR is also supported by previous reports on the efficacy of both techniques, tDCS [81,82,83] and VR [46, 51] applied individually. Importantly, additional improvements have been reported when they have been combined [77], as in this study, which has been argued to facilitate corticospinal excitability [44]. Although this possibility was not explored in the present study, the anodal stimulation over the ipsilesional motor cortex together with the concurrent involvement in the VR-based task and the subsequent participation in physical therapy could have facilitated the motor improvement detected in our participants. Interestingly, this paradigm has been proved to weaken the excitability of intracortical inhibitory circuits concurrently with practice, a phenomenon referred to as gating, which can increase the excitability of the motor cortex during motor learning [84]. The lack of a sham condition in the administration of the tDCS and the impracticability of providing a feasible placebo of the VR intervention could have influenced the effectiveness of the experimental intervention. However, the provision and strength of the sham condition in tDCS is still a matter of debate [85, 86].
The absence of motor changes evidenced by the four non-responders to the intervention are unlikely to be related to demographic nor clinical factors, as no differences in any variables were found that could explain the ineffectiveness of the intervention. We speculate that the absence of effect in these participants could rather be explained by a possible loss of corticospinal tract integrity. A pathological tract disruption could have affected the anatomic connectivity of white matter pathways [87], consequently affecting their motor function. In line with this, the fiber number ratio has been shown to have significant correlation with motor function, which, interestingly, is stronger in the chronic phase than in earlier phases [88]. Moreover, the integrity of the corticospinal tract is the second major predictor of upper limb recovery [9]. Unfortunately, as a limitation of the study, no structural nor functional data was available to check the integrity of the corticospinal tract of the participants, or to determine the effects of the intervention on cortical excitability or reorganization.
The clinical relevance of our results should be highlighted, based on the following considerations. First, all participants were chronic. The improvement detected in their motor function several months after stroke, where spontaneous neural recovery is unlikely [94], supports the effectiveness of the intervention. Previous reports on the effectiveness of combining tDCS and VR are focused on the acute phase post-stroke [77, 78] and, consequently, are unable to isolate the source of the improvement. Second, the participants also presented residual severe impairment in their upper limb motor function, which, as mentioned above, represents the worst scenario for functional recovery [9]. Third, the overcoming of the minimal clinically important difference in the improvement experienced by individuals who interacted with the combined tDCS and VR paradigm not only supports the relevance of the gains, but could also mandate a change in their clinical management [74]. Fourth, preliminary studies using a comparable protocol have also shown maintenance of gains in upper limb function one month after the intervention [53, 54], and a good acceptance [53]. And finally, the impressive improvement detected in this study provides support to the absence of a rehabilitation plateau, which has been previously suggested [95, 96], as the participants showed no benefits from physical therapy in the last two months prior to the intervention. The inexistent progress in this period might reflect an adaptation to the therapy, rather than being indicative of a diminished capacity for improvement. Inclusion in the experimental intervention could have helped them to overcome the adaptive state by modifying their regimen aspects using novel and different parameters and modalities [95].
This study investigated the effectiveness of a combined tDCS and VR-based intervention on upper limb function in individuals with chronic stroke and persistent severe hemiparesis. Our results provide evidence that a combined intervention, consisting of tDCS and a self-triggered motor observation exercise mediated by VR, produced clinically meaningful improvements in the motor function of those individuals compared to conventional physical therapy alone, while having similar effects on sensory function. 2ff7e9595c
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