SHORT COMMUNICATION

VISUALLY INDUCED KINAESTHETIC ILLUSION COMBINED WITH THERAPEUTIC EXERCISE FOR PATIENTS WITH CHRONIC STROKE: A PILOT STUDY

Ryosuke TAKAHASHI, MS1, Motoki KOIWA, MS1, Wataru IDE, MD2, Megumi OKAWADA, MS1,3, Kazuto AKABOSHI, MD, PhD3 and Fuminari KANEKO, PhD3,

From the 1Department of Rehabilitation, Hokuto Hospital, Obihiro, Hokkaido, 2Department of Neurosurgery, Hokuto Hospital, Obihiro, Hokkaido and 3Department of Rehabilitation Medicine, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan

Objective: Kinaesthetic perceptional illusion by visual stimulation (KINVIS) combined with neuromuscular electrical stimulation (NMES) and conventional therapeutic exercise (TherEX) has been shown previously to enhance motor function in stroke patients with chronic hemiparesis. The aim of this preliminary study is to assess the effects of a repetitive KINVIS intervention combined with TherEX, but without NMES, on upper limb motor function of patients with stroke-induced hemiparesis.

Design: A quasi-experimental study, with pretest–posttest for 1 group

Patients: Ten patients with stroke-induced, chronic, severe upper limb hemiparesis.

Methods: Patients were evaluated before and after a 10-day intervention, during which KINVIS and TherEX were applied for 20 and 60 min, respectively, for 5 days per week (Monday to Friday). Upper limb motor function was assessed using Fugl-Meyer Assessment (FMA) and Action Research Arm Test (ARAT), and resistance to passive movement in flexor muscles was assessed using the Modified Ashworth Scale (MAS). In addition, the amount of use and quality of movement of the affected upper limb in daily life were assessed using Motor Activity Log (MAL).

Results: Clinical assessments with FMA, ARAT, MAS, and MAL significantly improved after the intervention period.

Conclusion: A repetitive KINVIS intervention combined with TherEX may improve upper limb motor function in patients with chronic stroke and severe hemiparesis.

LAY ABSTRACT

Kinaesthetic perceptional illusion by visual stimulation (KINVIS) combined with neuromuscular electrical stimulation (NMES) and a conventional therapeutic exercise (TherEX) enhance muscle use in stroke patients with chronic paralysis. This preliminary study assessed the effects of a repetitive KINVIS intervention with added TherEX, but without NMES, on the use of the arm in Ten patients with stroke-induced paralysis. Ten patients with stroke-induced chronic paralysis were evaluated before and after a 10-day intervention, during which KINVIS and TherEX were applied for 20 and 60 min, respectively, for 5 days per week (Monday to Friday). The use of the paralysed arm improved significantly after the intervention. The repetitive KINVIS intervention combined with TherEX may improve the use of the arm in patients with chronic paralysis due to stroke.

Key words: stroke; upper limb motor function; rehabilitation; augmented reality; illusion.

 

Citation: J Rehabil Med 2022; 54: jrm00276 DOI: http://dx.doi.org/10.2340/jrm.v54.29

Copyright: © Published by Medical Journals Sweden, on behalf of the Foundation for Rehabilitation Information. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/)

Accepted: Feb 15, 2022; Epub ahead of print: Feb 22, 2022; Published: Apr 7, 2022

*Correspondence address: Fuminari Kaneko, Department of Rehabilitation Medicine, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. E-mail: f-kaneko@keio.jp

Competing interests and funding: FK is the founding scientist of the start-up company INTEP Inc. for the social implementation of university research results. This company does not have any relationship with the device or setup used in the present study. FK received license fees from Inter Reha Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

 

Upper limb motor dysfunction is a common problem in stroke patients. It disrupts the patient’s activities of daily living (ADL) and reduces their quality of life (QOL). Kinaesthetic perceptional illusion by visual stimulation (KINVIS) can be applied as a neurorehabilitation approach, which restores the upper limb motor function in post-stroke survivors. KINVIS is defined as a psychological phenomenon in which a resting person feels as if their own body part is moving or feels the desire to move a body part while watching a video of the same body part being moved (1). This is a implicit motor imagery that is carried as a result of cognitive substitution of the paralysed real body with a functioning virtual body. We have demonstrated previously that primary motor cortex excitability is increased during KINVIS (1). Moreover, previous studies have shown that motor-related areas are activated when experiencing KINVIS more than during simple observation of a similar movement (2). The psychological experiences in KINVIS and neurological effects may contribute to recovering post-stroke upper limb motor dysfunction. KINVIS has been shown to immediately improve motor function in patients with chronic stroke exhibiting severe hemiparesis (3).

We reported recently that an intervention of combined KINVIS and neuromuscular electrical stimulation (NMES), in addition to conventional therapeutic exercise (TherEX) for 10 days, positively influenced upper limb motor function in chronic stroke patients with severe hemiparesis (4). However, we believe that the repetitive application of the KINVIS intervention without NMES may have a beneficial effect on motor function in patients with chronic stroke. The aim of the current pilot study was therefore to clarify the impact of a repetitive KINVIS intervention without NMES, but in combination with TherEX, on upper limb motor function in chronic stroke patients with severe hemiparesis.

METHODS

Study design

This was a non-randomized, quasi-experimental study, with pretest–posttest for 1 group.

Participants

Ten patients with hemiparetic stroke were included in the study. The inclusion criteria were: (i) stroke impairment assessment set (5) of the distal (finger function) score of 0 or 1A (a score of 1A is assigned for gross finger flexion and 0 for a complete lack of voluntary finger movement); (ii) period from stroke onset of > 6 months; (iii) patients older than 18 years; and (iv) patients who have not received special rehabilitation or treatment for upper limb hemiparesis, such as transcranial magnetic stimulation, repetitive facilitative exercise, and botulinum toxin within the last 3 months. Exclusion criteria were: (i) inability to understand the purpose and task of the study; and (ii) presence of severe internal disorders of the heart and metabolism. All patients provided written informed consent to participate in the study. The study was approved by the local ethics committee of our institution (Hokuto Hospital, Obihiro, Japan), conformed to the principles of the Declaration of Helsinki, and was registered as a clinical trial with the University Hospital Medical Information Network in Japan (UMIN Clinical Trial Registry UMIN000035985).

Interventions

The experimental period was 10 days (2 weeks) of intervention on weekdays (Monday to Friday), and evaluations were performed before and after each intervention (Fig. 1). The intervention included KINVIS (20 min), followed immediately by TherEX (60 min), as described previously (4).

Figure 1
Fig. 1. (A) Study plan outline. The study comprised 10 days of intervention on weekdays, and evaluations were conducted before and after the intervention. The intervention included kinaesthetic perceptional illusion by visual stimulation (KINVIS) and conventional therapeutic exercise (TherEx). The KINVIS intervention was applied for 20 min, and TherEx was applied after KINVIS intervention for 60 min. (B) KINVIS intervention setup. Upper left: the KINVIS intervention used the KiNvisTM System, which consists of a table with 2 monitors and a chair for the patient to sit on. Upper right: hand movement on the unaffected side was recorded once using the KiNvisTM System camera before the intervention. Lower left: the video-recording of the unaffected side was flipped using the KiNvisTM System to mirror the movement of the affected side. Lower right: their arm was supported on a stand to avoid somatosensory input.

KINVIS

KINVIS was applied for 20 min using the KiNvisTM System (IP-KINVIS-HT01, Inter Reha Co., Ltd, Tokyo, Japan) (4). Patients were seated on a chair with their forearms on the table. The hand movement of the unaffected side was recorded once using the KiNvisTM System camera before the intervention. The hand movement task involved opening and closing the hand on the unaffected side. The recorded video of the unaffected side was flipped using the KiNvisTM System to mirror the movement of the affected side, and the flipped video was adjusted such that the forearm in the video overlapped with the patient’s actual forearm from the patient’s viewpoint. Their arm was supported on a stand to avoid somatosensory input. During the KINVIS intervention, patients were instructed to relax and to not move either hand. KINVIS intervention was applied as 2 sets of 10 min each for a total of 20 min per week day (Monday to Friday).

TherEX

TherEX was applied for 60 min/session/day by a physical or occupational therapist after the KINVIS intervention. TherEx consisted of stretching, muscle strength training. Individual exercises for the upper limbs were selected for each patient to gradually increase the difficulty level using a graded approach.

Clinical evaluations

The clinical assessments included measurements of upper limb motor function, resistance to passive movement of the flexor muscles, and actual use of the affected upper limb in ADL. The Fugl–Meyer Assessment (FMA) scale was used to assess upper limb motor impairment (6). This test consisted of shoulder/elbow/forearm, wrist, hand movement, and coordination/speed assessment. The FMA upper limb motor score ranges from 0 to 66. The Action Research Arm Test (ARAT) was used to reflect activity capacity (7) and consists of 4 components: grasp, grip, pinch, and gross movements. The Modified Ashworth Scale (MAS) was employed to assess resistance to passive movement in the elbow flexor and wrist flexor muscles (8). The MAS is an original scale with scores of 0, 1, + 1, 2, 3 and 4. This assessment scale provides high reliability for measuring the upper extremities (8). The Motor Activity Log (MAL) assesses the upper limbs’ actual perceiver activity performance in ADL (9). The MAL consists of 2 components: the amount of use (AOU) and quality of movement (QOM). Both AOU and QOM scores ranged from 0 to 5.

Data analysis

To calculate the median value of the MAS scores, score 1+ was transposed to 2, and scores 2, 3, and 4 were transposed to 3, 4, and 5, respectively. The Wilcoxon signed-rank test was used to compare clinical assessments before and after the intervention. The statistical level of significance was 5% (p < 0.05). All statistical analyses were performed using statistical software (SPSS Statistics version 20, IBM, Armonk, USA).

RESULTS

Ten patients (8 males, 2 females; 7 with left hemiparesis and 3 with right hemiparesis; mean age 67.7 ± 7.9 years; mean height 164.3 ± 5.9 cm; mean weight 63.8 ± 9.2 kg) with hemiparetic stroke were included. All participants were right-handed, as indicated with the Edinburgh Handedness Inventory test (group scores 94.5 ± 11.8%). Participant demographics and clinical characteristics are shown in Table I. The results of the clinical assessments are shown in Table II. In addition, Fig. 2 shows changes in the clinical assessments for each participant and score distribution. Regarding FMA, the Upper Extremity Motor (p = 0.005), Shoulder/Elbow/Forearm (p = 0.007), and Hand scores (p = 0.026) improved following the intervention. The total ARAT score increased, as did the Grasp score (total score: p = 0.027, Grasp: p = 0.027). The MAS scores of the paretic side at the wrist flexors decreased (p = 0.005). Furthermore, the AOU and QOM scores of MAL increased among the participants (AOU: p = 0.005; QOM: p = 0.005).

Table I. Demographic and clinical characteristics of patients
Patient Sex Diagnosis Lesion Location Age (Years) Paretic Side TFO(Months) SIAS U/L
Proximal Distal
1 male CH Putamen, Capsule internal 73 Lt 254 2 1A
2 male CI Capsule internal 74 Lt 7 1 1A
3 male CI Corona radiata, Insula, Putamen, Pallidum 66 Lt 93 2 1A
4 male CI Corona radiata, Insula, Putamen, Pallidum, Precentral gyrus 72 Lt 205 3 1A
5 male CH Precentral gyrus, Corona radiata, Insula, Putamen, Pallidum 65 Rt 76 2 1A
6 male CH Putamen, Capsule internal 67 Lt 32 3 1A
7 female CH Precentral gyrus, Corona radiata 47 Rt 26 0 0
8 male CI Precentral gyrus, Corona radiata, Insula, Putamen, Pallidum 72 Rt 137 0 0
9 male CH Putamen, Capsule internal, Pallidum 72 Lt 75 2 0
10 female CH Putamen, Capsule internal, Pallidum 69 Lt 16 2 1A
Abbreviations: CI, cerebral infraction; CH, cerebral hemorrhage; Rt, right; Lt, left; TFO, time from onset of stroke; SIAS, Stroke Impairment Assessment Set; U/L, Upper Limb.
A score of proximal; If a patient is able to touch his contralateral knee with his affected hand and bring it back to his mouth, a score of 3 is given. When the patient can only lift the hand to the level of the nipple, a score of 2 is given. If there is no muscle contraction noted in the biceps brachii, a score of 0 is given.
A score of distal; A score of 1A is given for gross finger flexion, and 0 is assigned for a complete lack of voluntary finger movement.
Table II. Clinical assessments of the upper limb
Before After Z-value p-value
Median [IQR] Median [IQR]
FMA
 Upper extremity total score 13.0 [10.3-16.0] 15.5 [12.5-19.5] 2.83 0.005 **
 Shoulder / Elbow / Fore-arm 12.5 [9.0-14.8] 14.5 [10.5-17.5] 2.71 0.007 **
 Wrist 0.0 [0.0-0.0] 0.0 [0.0-0.0] 1.00 0.317
 Hand 1.0 [0.3-2.0] 2.0 [1.3-2.0] 2.22 0.026 *
 Coordination / Speed 0.0 [0.0-0.0] 0.0 [0.0-0.0] - -
ARAT
 Total score 3.0 [3.0-3.8] 5.5 [3.0-6.8] 2.21 0.027 *
 Grasp 0.0 [0.0-0.0] 1.0 [0.0-3.5] 2.21 0.027 *
 Grip 0.0 [0.0-0.0] 0.0 [0.0-0.0] 1.00 0.317
 Pinch 0.0 [0.0-0.0] 0.0 [0.0-0.8] 1.60 0.109
 Gross movement 3.0 [3.0-3.8] 3.0 [3.0-3.8] - -
MAS
 Elbow flexor muscles 2.0 [2.0-2.0] 2.0 [1.3-2.0] 1.00 0.317
 Wrist flexor muscles 2.5 [2.0-3.0] 1.5 [1.0-2.0] 2.83 0.005 **
MAL
 Amount of use 0.0 [0.0-0.1] 0.6 [0.3-0.7] 2.80 0.005 **
 Quality of movement 0.0 [0.0-0.1] 0.4 [0.3-0.7] 2.80 0.005 **
Abbreviations: FMA, Fugl-Meyer assessment scale; ARAT, Action research arm test; MAS, Modified ashworth scale; MAL, Motor activity log; IQR; interquartile range. *, p < 0.05 and **, p < 0.01. For the FMA coordination / speed score and the ARAT gross movement score, the p-value was not calculated because of the same value before and after the intervention for all participants.

Figure 2
Fig. 2. Changes in clinical assessments in each participant. The line graph shows the changes before and after the intervention in each participant. The lines in the graphs are displaced to avoid overlap. However, Fugl-Meyer Assessment (FMA) (wrist, hand, and coordination/speed), Action Research Arm Test (ARAT), and Modified Ashworth Scale (MAS) appear blank or have a small number of lines because some participants had zero or the same points before and after the intervention.

DISCUSSION

This investigation prospectively assessed the effect of a repetitive KINVIS intervention, followed by immediate TherEX on motor function in patients with stroke exhibiting severe hemiparesis. Clinical assessments with FMA, ARAT, MAS, and MAL demonstrated significant improvement after the therapeutic intervention period. This finding indicates that, in patients with stroke exhibiting severe hemiparesis, resistance to passive movement of the flexor muscles of the wrist had reduced, and the motor function of the upper limb, including the finger, had improved following the intervention. Therefore, a repetitive KINVIS intervention combined with TherEX may have a positive effect on upper limb motor function in stroke patients. Moreover, it was hypthesized that these upper limb function changes increased MAL by employing the paralysed upper limb for ADL. Thus, a repetitive KINVIS intervention combined with TherEX may have a positive effect on upper limb motor function in chronic stroke patients with severe hemiparesis. Although the total score of FMA and ARAT significantly increased, the median increase was 2.5 points, which was a small change. Hence, research that uses a larger sample size and confirms the effect size as a future prospect is necessary.

This study enrolled chronic stroke patients with severe hemiparesis, similar to a previous study that combined the KINVIS intervention and NMES (4). The KINVIS intervention effectively promotes motor learning (10). We found that the KINVIS intervention positively influenced upper limb motor function, even in the absence of NMES. According to a previous study involving healthy participants, increased cortical excitability was sustained when KINVIS was combined with peripheral nerve stimulation, rather than when the KINVIS intervention was used alone (11). Therefore, in terms of brain plasticity, the combination of KINVIS and NMES may be superior to the KINVIS intervention alone. However, this study did not draw comparisons from the combined KINVIS and NMES intervention. In the previous study combining the KINVIS intervention and NMES (4), the mean values of the total FMA score (before: 12.2 ± 2.9; after: 14.5 ± 4.0) and the total ARAT score (before: 5.3 ± 4.4; after: 8.1 ± 7.6) for the upper extremity increased by approximately 2.0–3.0 points after the intervention. Therefore, the upper limb motor function changes are comparable between this study and the previous study. Although the present study and the previous study (4) cannot be compared because of their sample size and the non-homogeneous sample populations. Therefore, the extent of the clinical implications of these differences in intervention methods remains unclear, and further research into this subject is necessary.

Mirror therapy is an intervention that is seemingly similar to the KINVIS intervention adopted in this study. A Cochrane review (12) reported that mirror therapy moderately improved motor function and ADL. In addition, mirror therapy has a small effect on the upper extremity total FMA score. In the current study, we also noted an increase in the FMA, ARAT total scores, and MAL, which may have positively affected upper limb motor function and ADL as well as mirror therapy. The difference in the results between the report for the mirror therapy and the current study was due to the effect on MAS. For mirror therapy, absence of the effect on MAS was demonstrated (13); however, improvement in MAS was one of the main effects of KINVIS in this study. The kinaesthetic illusion during the mirror therapy is not a purely visually induced illusion, but emerges from proprioceptive afferents of the contralateral moving arm (14). In contrast, the kinaesthetic illusion during our intervention is induced only by visual input without the contralateral upper limb movement. Therefore, the mechanisms of KINVIS intervention and mirror therapy were different. This difference in mechanism may result in different effects on patients with hemiplegic stroke. This will be the topic of a future study.

Despite the favourable outcomes of this study, it has some limitations. First, the study lacked a control group. Although the FMA and ARAT total scores in this study improved, the sub-scores of the FMA showed a significant increase in the scores of shoulder/elbow/forearm as well as the hand. Strength training for stroke hemiplegic cases reportedly improves upper limb motor function (15). Therefore, changes in this study may have been influenced by TherEx. Secondly, participants had chronic (with an onset period of ≥ 6 months) stroke, but with variations from 7 to 254 months. Hence, it was not possible to fully infer the effectiveness of the KINVIS intervention as a therapeutic manoeuvre. A randomized controlled study is therefore needed to explore the possibility of using the KINVIS intervention as a therapeutic intervention tool for improving upper limb motor function in stroke patients.

In conclusion, these preliminary results showed that a repetitive KINVIS intervention combined with TherEX might improve upper limb motor function in chronic stroke patients with severe hemiparesis. Nevertheless, as this study has several limitations, further investigations are required to validate the likely benefit of this approach in stroke patients with severe upper limb hemiparesis.

ACKNOWLEDGEMENTS

The authors thank all the patients who participated in the study.

REFERENCES

  1. Kaneko F, Yasojima T, Kizuka T. Kinesthetic illusory feeling induced by a finger movement movie effects on corticomotor excitability. Neurosci 2007; 149: 976–984.
  2. Kaneko F, Blanchard C, Lebar N, Nazarian B, Kavounoudias A, Romaiguère P. Brain regions associated to a kinesthetic illusion evoked by watching a video of one’s own moving hand. PLoS ONE 2015; 10: e0131970.
  3. Kaneko F, Inada T, Matsuda N, Shibata E, Koyama S. Acute effect of visually induced kinesthetic illusion in patients with stroke: a preliminary report. Int J Neurorehabil 2016; 3: 212.
  4. Kaneko F, Shindo K, Yoneta M, Okawada M, Akaboshi K, Liu M. A case series clinical trial of a novel approach using augmented reality that inspires self-body cognition in patients with stroke: effects on motor function and resting-state brain functional connectivity. Front Syst Neurosci 2019; 13: 76.
  5. Tsuji T, Liu M, Sonoda S, Domen K, Chino N. The stroke impairment assessment set: its internal consistency and predictive validity. Arch Phys Med Rehabil 2000; 81: 863–868.
  6. Fugl-Meyer AR, Jääskö L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med 1975; 7: 13–31.
  7. Yozbatiran N, Der-Yeghiaian L, Cramer SC. A standardized approach to performing the action research arm test. Neurorehabil Neural Repair 2008; 22: 78–90.
  8. Meseguer-Henarejos AB, Sánchez-Meca J, López-Pina JA, Carles-Hernández R. Inter- and intra-rater reliability of the modified ashworth scale: a systematic review and meta-analysis. Eur J Phys Rehabil Med 2018; 54: 576–590.
  9. Van der Lee JH, Beckerman H, Knol DL, W de Vet HC, Bouter LM. Clinometric properties of the motor activity log for the assessment of arm use in hemiparetic patients. Stroke 2004; 35: 1410–1414.
  10. Nojima I, Koganemaru S, Kawamata T, Fukuyama H, Mima T. Action observation with kinesthetic illusion can produce human motor plasticity. Eur J Neurosci 2015; 41: 1614–1623.
  11. Kaneko F, Takahashi R, Shibata E. Paring of kinesthetic illusion induced by visual stimulus and peripheral nerve stimulation causes sustained enhancement of corticospinal tract excitability. Clin Neurophysiol 2017; 128: e167.
  12. Thieme H, Morkisch N, Mehrholz J, Pohl M, Behrens J, Borgetto B et al. Mirror therapy for improving motor function after stroke. Cochrane Database Syst Rev 2018; 7: CD008449.
  13. Yavuzer G, Selles R, Sezer N, Sütbeyaz S, Bussmann JB, Köseoğlu Fet al. Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil 2008; 89: 393–398.
  14. Chancel M, Brun C, Kavounodias A, Guerraz M. The kinaesthetic mirror illusion: How much does the mirror matter? Exp Brain Res 2016; 234: 1459–1468.
  15. Harris JE, Eng JJ. Strength training improves upper-limb function in individuals with stroke. Stroke 2010; 41: 136–140.