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Mirror Illusion for Sensori-Motor Training in Stroke: A Randomized Controlled Trial
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Mirror Illusion for Sensori-Motor Training in Stroke: A Randomized Controlled Trial Kamal Narayan Arya, MOT, PhD,* Shanta Pandian, MOT,* Vikas, BOT,* and Vinod Puri, DM† Background: Poststroke, sensory deficits are not uncommon. In spite of the close association between the sensory and motor recovery, the deficits are usually underemphasized. Mirror therapy (MT), a neural-based approach for the motor deficit has not been explored for the sensory impairment. The objective of the present study was to develop and determine the effect of a MT program for sensori-motor impairment among poststroke subjects. Methods Design: Randomized controlled trial. Setting: Functional therapy laboratory of Rehabilitation Institute. Participants: Thirtyone chronic poststroke subjects (17 experimental and 14 controls), aged between 30 and 60 years, with diminished light touch in the hand. Outcome Measure: Semmes Weinstein Monofilament (cutaneous threshold), 2-Point discrimination test (touch discrimination) and Fugl-Meyer Assessment (hand motor recovery). Intervention: The experimental group received sensory stimulus such as tactile perception and motor tasks on the less-affected hand using mirror box. The control counterparts underwent only dose-matched conventional program. 30 sessions with a frequency of 5/week were imparted to the groups. Results: Post intervention, there was a significant (P < .004) increase up to 30% positive touch-response for the hand quadrants among the experimental group in comparison to only 13.5% rise for the same among the controls. The cutaneous threshold of the less-affected palm also improved significantly among the experimental subjects in comparison to the controls (P = .04). Conclusion: MT may be considered as a promising regime for enhancing cutaneous sensibility in stroke. The mirror illusion induced by MT may be utilized for sensory and motor deficits as well as for the more-affected and less-affected hands. Key Words: Cerebrovascular accident—Cutaneous threshold—Hand— Monofilament—Rehabilitation—Tactile—2-point discrimination © 2018 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction Sensory impairment is not uncommon after stroke; however usually not emphasized due to the apparent motor paresis.1 The somatosensory deficits are not only From the *Pandit Deendayal Upadhyaya National Institute for Persons with Physical Disabilities, New Delhi, India; and †Department of Neurology, GB Pant Post Graduate Institute of Medical Education and Research, New Delhi, India. Received May 16, 2018; revision received June 27, 2018; accepted July 5, 2018. Financial disclosure: Indian Council of Medical Research, 5/4-5/2/ ADR/2014-NCD-I, New Delhi, India for financial assistance. Address correspondence to Kamal Narayan Arya, MOT, PhD, Pandit Deendayal Upadhyaya National Institute for Persons with Physical Disabilities, New Delhi, India. E-mail: [email protected] 1052-3057/$ - see front matter © 2018 National Stroke Association. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jstrokecerebrovasdis.2018.07.012
presented on the contralateral body side to the brain lesion but also on the ipsilateral side.2 The sensory recovery has been found to be strongly associated with the level of the motor recovery.3 Further, the sensory deficit affects quality of life among stroke subjects.4 Up to 85% of the subjects could experience sensory deficits. The individual may exhibit deficit in tactile, propriopception, vibration, steregnosis, and 2-point discrimination abilities.5,6 The sensory deficits hamper the ability to utilize the available motor level in the functional tasks.7 Thus, adequate motor recovery depends upon the intact sensation.8-10 The impaired sensation along with the complex motor deficits increases the disability manifold.6,11 In a lesioned brain, the motor control is facilitated by alternative sensorimotor pathways recruited from secondary motor areas. Poststroke sensory deficits are the consequence of structural damage of cortical and subcortical structures. The primary somatosensory area situated in
Journal of Stroke and Cerebrovascular Diseases, Vol. &&, No. && (&&), 2018: pp 1–11
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the postcentral gyrus is commonly affected regions.6,12 Thalamus and basal ganglia are the most crucial areas which coordinate sensory information with motor cortex. Usually, thalamic stroke is supposed to be sensory stroke; whereas clinically a diversity of sensory loss presentation has been observed among other lesions also.13,14 The identification and assessment of sensory issues in poststroke subjects are still under explored. The apparent motor impairment in contrast to the subtle sensory deficits could be the reason for overlooking the issue. Additionally, stroke specific sensory outcome measures are sparsely available.6,15 In poststroke, sensory training of varied range has been investigated.5,6,16 The techniques may range from passive techniques such as somatosensory electrical stimulation to active retraining of stereognosis, proprioception, discriminating, and localizing sensations.16,17 The other investigated sensory interventions are sensory electrical stimulation, thermal stimulation, and pneumatic compression technique. However, none of them exhibited sufficient evidence for their effectiveness.5,6 Further, sensory and motor techniques have also been combined to explore the response of upper limb function. It has been suggested to amalgamate the techniques to enhance the upper limb recovery.18 Techniques such as mirror Therapy (MT) have been developed for motor rehabilitation in stroke.19 MT provides a form of visual illusion by watching the reflection of the unaffected limb on a mirror. The patient performs movement of the unaffected limb and creates an image of the affected limb in a mirror.20,21 The illusion enhances the interhemispheric communication as well as activity of the certain brain areas associated with the motor performance of the affected limb. Various mechanisms have been proposed to be responsible for MT including mirror neuron system.22 MT using tasks has been proven to be an effective technique for the upper limb rehabilitation among stroke patients.20-22 Although activity or task-based MT unquestionably utilize sensations to complete the task, the technique has not been explored for sensory rehabilitation. It is evident that sensory and motor functions are interlinked in healthy and lesioned brain.23,24 Integration of sensory abilities is crucial for the recovery of motor control and motor learning.1,25,26 However, the sensory intervention has been underemphasized due to motor rehabilitation.1 Poststroke, both the functions gets impaired and recovered together.4,5,27-29 However, till today, all the stroke rehabilitation methods have developed exclusively for the motor aspect. A novel treatment training to treat sensory and motor impairments needs to be developed. The objective of study was to develop a MT program using tasks for sensory and motor impairment and to determine the effect of the protocol on sensory and motor recovery among poststroke survivors.
Methods The present study followed the CONSORT (Consolidated Standards of Reporting Trials) guidelines for the nonpharmacologic treatments.30 The protocol of the study was approved by the Institutional Ethics Committee of Pandit Deendayal Upadhyaya National Institute for Persons with Physical Disabilities. The informed signed consent was obtained from all the enrolled participants. The potential subjects were recruited from a nationallevel rehabilitation institute situated in an urban city. The investigation was conducted in a functional therapy laboratory of the institute. The participants were enrolled in the study if they met the following inclusion criteria: (i) unilateral stroke of >6 months, (ii) hemiparesis of right or left side, (iii) age between 30 and 60 years, and (iv) sensory deficit in the palamar aspect of the hand and fingers (assessed by the Semmes-Weinstein monofilaments as diminished light touch).24,31 However, the subjects were excluded if they exhibited any of the following: (i) cognitive and perceptual deficits (determined clinically by trail making test, digit span, copying and drawing, line-bisection, and functional performance), (ii) receptive communicative disorder, (iii) contracture of hand muscles or any fixed wrist/hand/finger deformity, (iv) complex regional pain syndrome, (v) diabetic or any other type of neuropathy, and (vi) skin disorder affecting the upper limb. The study was a randomized controlled, assessor blinded trial. Sample size was not calculated for the study as no MT study was found using sensory measure as a primary outcome. The subjects were not blinded due to nature of the intervention. The selected subjects were randomly divided into the experimental and control group using computer generated random numbers. The randomization procedure was performed by a research assistant who was not concerned with the present study. The allocation of intervention was divided in the ratio of 1:1 and that was serially arranged in sealed opaque paper envelopes. After getting signed written informed consent, the subjects were enrolled for the study. The experimental group subjects received 30 sessions, 40 minutes each across the 6 weeks (5/week). Additionally, 50 minute conventional occupational therapy was also provided. The rationale for providing the conventional therapy to the experimental group was to avoid deprivation of the affected upper limb from the motor and sensory training. The control group subject received only standard motor and sensory rehabilitation; however, for 90 minutes duration to match the total dosage of therapy between the groups. Specifically, the experimental participants received task-based mirror therapy using the mirror frames or mirror box (dimensions and purpose are provided in the Box 1). The mirrored wall of the frame/box was placed vertically along the midsternum level. The affected limb was hidden beside the nonreflective side of the wall. The subjects were provided sensory stimulus (various textures, size, and
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Box 1. Type of mirror
Dimension
Purpose
Short mirror frame (Table mounted) Mirror box (Wooden)
18 £ 16 inches
Used for sensory intervention, as both the sides are free to provide sensory stimulus Used for the wrist and hand movements
24 £ 18 £ 14 inches
Box 2. Sensation
Intervention
Light touch Vibration
Piece of cotton/tissue paper were lightly touched or stroked on the all quadrants of hands. Electrical motorized toothbrush was used to provide stimulation from the fingers to palm in distal to proximal pattern. Blunt end of a pen was touched at the different points on the hands
Tactile localization Stereognosis Recognition of texture
Recognition and manipulations of various familiar objects. Hard to soft material was used in order (scrubber, steel wool, metal, washing brush, denim cloth, wool, cotton ball).
shape) on the less-affected and the affected hands simultaneously to induce mirror illusion for sensory perception (Box 2) (Fig 1). The stimulus was provided in 2 ways: selfperception and passively applied by the therapist. The self-perception of the stimulus was performed bilaterally by the higher motor stage subjects else unilaterally by the less-affected side. For stereognosis, object recognition was performed without vision occlusion. Each sensory stimulus was imparted for 2-5 minutes to a total of 20 minutes. The participants were also provided need-based auditory feedback and stabilization of the paretic limb (by another therapist). The practice of paretic wrist and hand using various tasks were also conducted as MT (Box 3). The motor tasks were selected as per the specific impaired items of Fugl-Meyer assessment (wrist-hand). Simultaneous bilateral movements (more-affected hand without task) were preferred; however, for lower motor stage
subjects only unilateral performances were allowed. The movements were provided in repetition of 20-50 to a total of 20 minutes. Sensory stimuli of similar sensations on the affected hand and neurophysiological based motor rehabilitation were also imparted as conventional therapy.
Primary Outcome Measures Semmes Weinstein Monofilament Semmes-Weinstein monofilaments (SWM) are precisely calibrated nylon filaments used to measure diminished cutaneous sensation. The monofilament sets ranged from normal, diminished light touch, diminished protective sensation, and loss of protective sensation.31 The monofilament test has been used in other stroke studies to measure the sensory deficits.24,32 In the present study, to have
Figure 1. The left hemiparetic subject receiving sensory stimulus (rough texture) simultaneously on both the sides using mirror frame. The illusion of right hand has been created which is perceived as the left hand.
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Box 3. S. No.
Movement
Activity
1. 2. 3. 4. 5. 6. 7. 8.
Wrist Wrist Wrist Wrist Fingers Fingers Fingers Fingers
Dorsiflexion 0-30˚ using cylindrical block Stability at 15˚; holding soft ball Repeated dorsiflexion / palmar flexion using cylindrical block Circumduction; making a circle by pen Flexion/extension; ball squeezing Clay activity (kneading) Clay activity (making balls) Zymkit activity
a comprehensive sensory status, the assessment was conducted on the entire hand (palmar aspect) by dividing it into the 30 quadrants (Fig 2).33 The filaments were applied on each quadrant to score the positive response for the most sensitive to crude filaments, cutaneous threshold force ranging from .0045 to 447 g (.0045-.0677 g=normal sensation, .1660-.4082 g=diminished light touch, .69582.0520 g=diminished protective sensation, 3.632-447 g=loss of protective sensation).
2-Point Discrimination The static 2-point discrimination (2PD) test was applied using the modified vernier caliper with blunted extension. The scoring is done in mm based on the ability to perceive the 2 points being touched simultaneously. The testing was conducted on all the 30 quadrants of hand. The normal scores were considered as 3 mm, 4-5 mm, 6-7 mm, and 710 mm, respectively for the distal phalanx, middle phalanx, proximal phalanx, and palm.33 The test has been found to be a reliable measure and used in poststroke subjects.34,35 Both SMF and 2PD were also measured on the lessaffected hand for the additional reference value. In addition to above measures, the other somato-sensory abilities such as pain, temperature, stereognosis were assessed clinically as a part of standard rehabilitation assessment.33,36
Secondary Outcome Measure Fugl-Meyer Assessment (FMA) Fugl-Meyer's assessment (FMA) assesses the poststroke motor recovery in a hierarchically organized pattern. The motor items primarily comprise reflexive, synergistic, outof-synergy, movements. The 33-item upper extremity section is scored on 3-point ordinal scale ranging from 0 (no performance) to 2 (faultless performance) with a maximum score of 66. The section further has 2 components; upper arm and wrist-hand (FMA-WH) with sub score of 36 and 30, respectively. FMA has been widely used in poststroke studies since decades and found to be a reliable and valid measure.37-40 Subsection FMA-WH has been used in the present study.
Data Analysis The data analysis was performed using IBM SPPS version 23. The analysis of covariance (ANCOVA) was carried out to determine the difference between the experimental and control groups for the SWM and FMA measures. The median score for each finger/palm unit were considered for mean calculation of the sample. Since the maximum cutaneous force threshold measured by SWM was 447 g, the score of 448 g was awarded for the
Figure 2. Sensory assessment of the right paretic hand using Semmes Weinstein Monofilamens on 30 testing quadrants mapped on hands.
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Figure 3. Flow chart of the study.
quadrants responded not even to the crudest filament. Further, the number of positive responses for each cutaneous threshold force as assessed by the SWM was calculated to assess the pre and post intervention changes. The total positive response respectively for the palm and finger were 238 (17 subject £ 14 finger quadrant) and 272 (17 subject £ 16 palm quadrant) among the experimental subjects whereas 196 (14 subject £ 14 finger quadrant) and 224 (14 subject £ 16 palm quadrant) in the control group. Chi-square test was used to compare the responses between the groups. The median value for the finger (14 quadrants)/palm (16 quadrants) for each participant was considered for the analysis of the 2PD measures. The conventional value of P < .05 was considered as the level of significance.
Results Eighty-nine subjects were screened for the enrollment out of which 58 either did not meet the eligibility criteria or did not agree to participate in the study. Thirty-one participants were randomly divided into the experimental (n = 17) and control (n = 14) groups. Figure 3 shows the flow of participants throughout the study. One control subject discontinued the intervention after few sessions and an experimental subject did not report for the post assessment. All other subjects completed the protocol of the study. The average age of the study participants was 46 years with 26(84%) males. The mean post stroke duration was 15 months with 14(45%) subjects with ischemic stroke. Seventeen (55%) and 14 (45%) subjects were at
Brunnstrom recovery stage41,42 3 and 4, respectively. The other demographic details of the participants are mentioned in the Table 1. MT based sensory training was found to be feasible among all the participants. No adverse event was reported by any of the subjects. The average cutaneous threshold on the less-affected fingers and palm were .136 g (SD .111) and .457 g (SD .362), respectively for the experimental subjects whereas the same for the controls were .262 g (SD .219) and .457 g (SD .388), respectively. The mean cutaneous threshold on the affected fingers and palm were 346.08 g (SD 189.52) and 346.58 g (SD 188.39), respectively for the experimental group. The same for the controls were 357.37 g (SD 180.88) and 357.43 g (SD 180.65), respectively. The threshold on the less-affected side (fingers .193; SD .177 and palm .457; SD .368) of all participants was significantly (P < . 001) lower than that on the affected side (fingers 351.18; SD 182.66 and palm 351.48; SD 181.94). Post intervention, the less-affected fingers of the experimental demonstrated same threshold whereas the palm exhibited the threshold of .442 g (SD .372). The change of palm was significantly (P = .04; 95% CI .008.0303) better than that of the control group (.598 g SD .552). The less-affected fingers of the control showed the threshold of .279 g (SD .225). The mean change in cutaneous threshold for the affected fingers and palm among the experimental subject were not found to be significant in comparison to that of the controls. Table 2a shows the pre and post mean changes for the SWM of the affected fingers and palm between the
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Table 1. Demographic and clinical characteristics of the participants S. No. 1. 2. 3. 4. 5.
6. 7. 8.
9.
10. 11. 12. 13. 14. 15.
Characteristic
Experimental group (n = 17)
Control group (n = 14)
Test statistics
Age (years) Mean § SD Time since stroke (months) Mean § SD Male/female (%) Socio-economic status (BPL/ LIG/MIG/HIG) Educational qualification (10th/12th/UG/PG) (%)
44.12 § 9.08 13.35 § 10.12
47.93 § 9.10 17.00 § 13.28
t:p = .191 t:p = .393
13(76.5%)/04(23.5%) 00(00%)/11 (65%)/6/(35%)/00(00%)
13(93%)/01(07%) 2(14%)/3(21%)/6(43%)/3(21%)
x2:p = .344
09(53%)/
05(36%)/
—
02(12%)/ 04(23.5%)/ 02(12%)/ 13(76.5%)/4(23.5%)
02(14%)/ 02(14%)/ 05(36%)/ 14(100%)/00(00%)
—
08(47%)/9(53%) 00(00%)/
6(43%)/08(57%) 00(00%)/
06(35%) / 01(6%) / 09(53%)/ 01(6%)
07(50%)/ 02(14%)/ 05(36%)/ 00(00%)
00(00%) 13(76.5%) 02(12%) 00(00%) 02 (12%) 02(12%) 9(53%)/8(47%)
00(00%) 14(100%) 02(14%) 02(14%) 05(36%) 00(00%) 9(64%)/5(36%)
— — x2:p = 1 — x2:p = .198 — x2:p = .717
17(100%)/0(0%)
14(100%)/0(0%)
—
2(12%)/6(35%) /4(23.5%) /5(29%) 6(35%)/4(23.5%)/4(23.5%) /3(18%) 10(59%) 00(00%)
6(43%)/3(21%)/3(21%)/2(14%) 9(64%)/3(21%)/0 (00%)/2(14%) 9(64%) 02(14%)
— — x2:p = .756 —
Marital status (married/ unmarried) Ischemic/Hemorrhagic (%) Area of involvement (Frontoparietal/basal ganglia/thalamus/multiple/others)
Risk factors Hereditary Hypertensive Chronic smokers Alcoholic Diabetes mellitus Obesity Side of involvement (Right/ left) (%) Dominant side (Right/left) (%) BRS-U (Stage 2/3/4/5) BRS-H (Stage 2/3/4/5) Shoulder support Hand splint
—
x2:p = .815 —
BPL, below poverty line; BRS- H, Brunnstrom recovery stage of hand; BRS-U, Brunnstrom recovery stage of arm; HIG, higher income group; LIG, lower income group; MIG, middle income group; PG, post graduate; SD, Standard deviation; UG, under graduate.
Table 2a. Pre- and postintervention changes on outcome measure among experimental and control groups Outcome measure
Pre-intervention
Difference between the means (95% CI)
F
P value
346.08 § 189.52 357.37 § 180.88 345.78 § 189.35 357.23 § 180.80
.068
.991
346.58 § 188.39 357.43 § 180.65 317.08 § 182.78 357.29 § 180.57
2.92
.098
Experimental group (n = 17)
SWM- Affected Fingers (Mean § SD) in g SWM- Affected Palm (Mean § SD) in g FMA-WH (Mean § SD)
Post-intervention
12.12 § 11.14
Control group (n = 14)
15.14 § 10.61
Experimental group (n = 17)
16.18 § 10.62
Control group (n = 14)
16.13 § 10.59
1.64¡4.23 6.01 <.001
CI, confidence interval; F, test value for ANCOVA; FMA-WH, Fugl-Meyer Assessment (Wrist-Hand); n, number; SD, standard deviation; SWM, Semmes-Weinstein monofilaments.
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groups. The detail about the number of positive (447 g)/no response (>448 g) for pre and post intervention for the total quadrants among the experimental and control groups is mentioned in the Table 2b. Post intervention, there was a significant (P = .004) increase of 27% positive responses for the finger quadrants among the experimental group in comparison to only 13.5% rise for the same among the controls. Similarly, the positive response for the palm increased significantly (P = .0001) by 30% in the experimental group whereas the same was only 14% among the controls. Only 8 (26%) subjects (4; 23.5% experimental and 4; 28.5% controls) responded to the 2PD testing on the affected side. The average 2PD in the finger and palm were 4.35 mm and 12.78 mm, respectively in the experimental group whereas 4.7 mm and 10.77 mm, respectively among the controls. Post intervention, there was increase of 3 (18%) subjects in the experimental group that could respond to 2PD test among the experimental group. All the subjects responded to the 2PD test on the lessaffected side. Both the groups exhibited average 2PD of 3.5 mm and 7 mm, respectively in the finger and palm. Further, after intervention the motor scores on FMAWH significantly (P < . 001) enhanced to 16.18 (SD 10.62) from 12.12 (SD 11.14) among the experimental subjects in comparison to the controls (16.13; SD 10.59 from 15.14; SD 10.61) (Table 2a).
Discussion Sensory ability is vital for an efficient motor performance. The hand sensibility is strongly related to the dexterous performance.43 The poor hand sensation also affects the motor control. In spite of the same level of motor paresis, the stroke subjects with sensory deficit are unable to induce appropriate force to avoid dropping of the object from the hand.24 The sensory impairment is also associated with the restriction in the participation resulting into a negative impact on daily life among post stroke survivors.44,45 Further, sensory training has neural basis, the therapy may induce cortical reorganization. In healthy individuals, sensory training led to the lateralization of sensory-motor cortical activity during task performance.46 MT may be considered as a promising technique in stroke rehabilitation. The present study demonstrated favorable changes in terms of number of the affected hand quadrants in response to MT. The technique allowed poststroke subject to experience normal sensory-motor perception of the paretic upper limb. The observation of normal hand movement may augment the strength of functional connectivity within the somatosensory cortex.47 The tactile inputs along with the visual feedback induce bilateral activation of primary sensory-motor cortex and secondary somatosensory cortex.48 The networking between the sensory and motor cortex also gets
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enhanced in response to MT.49 Also, MT based movements lead to immediate activation of the somatosensory cortex in comparison to the motor area.50 This could be the possible neural mechanism elucidating the effect of regime in the present study. In addition to this, the average cutaneous threshold on the affected hand of the experimental subject did not improve in comparison to the controls. This could be due to the severity of sensorymotor deficit among the participants. The subjects achieved cutaneous sensibility in some of the hand quadrants not all. On estimating the average of all the quadrants, the change in the threshold was found to be negligible. To our knowledge, this was the first study in which the sensory assessment was performed on the 30 hand segments. The minute evaluation explored the real extent of impairment as well as the pattern of recovery. The participants had low motor level and high sensory deficit. The low motor level has been found to be associated with the low cutaneous sensibility. However, the poor sensation may also be observed among mild paretic subjects.3 In the present study, 3 subjects with mild paresis had severely impaired sensations. MT technique has been explored and found to evident for motor and perceptual deficits.19,51,52 Exclusively sensory based MT in stroke has been sparsely explored. Although in a study,53 the effect of MT was evaluated for the sensory recovery; the intervention protocol was purely motor-based. The regime enhanced the sensory ability among the participants included on the basis of motor impairment only. The sensory impairment among chronic stroke subjects is evident. The subject with poor motor abilities experience more sensory deficit in comparison to those with the good control.3 However, the pattern of sensory recovery among acute or chronic stroke is conflicting.54 Further, the sensory recovery is related to the motor and functional recoveries.9,10,55 The association of sensory deficit and motor or functional outcome may increase with the chronicity.55 In the present study, the limited positive changes for the cutaneous threshold on the affected hand after the intervention could also be attributed to the intricate aspect of stroke rehabilitation.56 Since the subjects achieve positive changes on the certain hand quadrants rather than on the entire affected hand and had no goal regarding the target sensitivity, the success of the regime from the patient's perspective is questionable. In the present study, the less-affected side also exhibited sensory recovery after the experimental intervention. However, the control subjects did not receive any sensory stimulation on the less-affected side. The utilization of the less-affected side is the integral component of MT. The sensory stimulation to induce illusion for the affected side also provoked sensations on the less-affected side. The sensory issues such as tactile deficit on the less-affected side are also evident in the literature.2,11 MT has also been
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Table 2b. Cutaneous threshold (number of positive responses) pre and post intervention among the experimental and control groups Cutaneous threshold (g)
Preintervention: Fingers (14 quadrants) Experimental Control group group (n = 17) (n = 14) Total response- Total response17 £ 14 = 238 14 £ 14 = 196 150 46
0 0 0 8 20 0 0 0 0 2 0 0 6 12 8 0 0 0 0 0
4 3 0 4 3 0 0 0 1 1 2 1 3 2 0 12 10 0 0 0
x2:p = .988
116 122
123 73
36 15 0 8 20 0 3 3 0 2 0 0 8 10 8 0 9 0 0 0
4 3 1 20 13 0 0 0 1 1 2 0 0 0 0 16 12 0 0 0
Test statistics
x2:p = .004*
Experimental group (n = 17)
Control group (n = 14) Total response- Total response17 £ 16 = 272 14 £ 16 = 224 190 82
168 56
18 0 10 16 6 0 0 0 20 12 0 0 0 0 0 0 0 0 0 0
5 8 1 3 0 0 0 1 2 0 8 1 13 2 4 8 0 0 0 0
Test statistics
x2:p = .241
Postintervention: Palm (16 quadrants) Experimental Control group group (n = 17) (n = 14) Total response- Total response17 £ 16 = 272 14 £ 16 = 224 110 162
136 88
42 37 12 19 20 0 0 0 20 12 0 0 0 0 0 0 0 0 0 0
4 8 2 15 20 0 0 1 2 0 8 3 11 2 5 7 0 0 0 0
Test statistics
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*Significant † Highly significant
182 56
Experimental Control group group (n = 17) (n = 14) Total response- Total response17 £ 14 = 238 14 £ 14 = 196
Preintervention: Palm (16 quadrants)
x2:p = .0001y
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>447 447 Distribution of responses 447 g 447.0 281.5 127.0 75.00 29.00 15.00 11.70 8.65 5.50 3.632 2.0520 1.4940 1.1940 .6958 .4082 .1660 .0677 .0275 .0230 .0045
Test statistics
Postintervention: Fingers (14 quadrants)
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found to effective in enhancing the subtle motor impairment on the less-affected side.57 Furthermore, no evident protocol has been found for the management of the ipselesional sensory impairment. The discrimination ability, affecting hand function is not uncommon among the stroke subjects.58,59 In the present study, only few (26%) participants could respond to 2PD test; thus, the effect of intervention could not be analyzed. However, the range of 2-PD these participants could be utilized as reference value for further investigation. The experimental intervention also enhanced the motor recovery of the hand. Even short duration sensory intervention had a favorable implication on motor recovery. In a randomized cross-over trial, immediately after sensory stimulation such as vibration positive change on the hand function and reaching ability was observed.60 However, in a recent systematic review, there is a weak evidence for the sensory training facilitating the motor outcome.61 It is worthwhile to mention that the mechanism of MT is unique than the techniques used in the previous investigation. Although there are numerous sensory assessment tools in practice, no stroke specific sensory outcome is available. Scales such as Erasmus MC modification to the Nottingham Sensory Assessment has been recommended for the neurological conditions.62 However, the scale comprises the items for the entire body part not the specific hand segment.63 Considering the functional implication, a sensory measure should explore the hand evaluation in detail. Further, in the present study, SWM could only provide the measurement for the cutaneous threshold up to 447 g. The subjects who did not respond to the maximum force were awarded the score of 448 g for the purpose of analysis. The number of such responses was substantial that lead to the limited use of SWM. This further explains the less favorable results for the average change of SWM between the groups. Similarly 2PD has limited application in the present study; about 1/4th of the subjects could response to the test. The discrimination ability in the hand/fingers of the majority of the subjects was absent. Since 2PD test is scored as the minimum distance between the touch stimuli, it does not have any scoring provision for the absence of the discrimination ability. Thus, ANCOVA was not utilized for the 2PD analysis. Sensory assessment and management is considered to be vital by the practitioners. However, the evidence-based clinical application is sparse in stroke rehabilitation.15 The present study provides a novel method of sensory intervention not only for the more-affected hand but also for the less-affected side. Additionally, MT, a versatile method simultaneously acts on the motor deficit. The negligible number of female subjects (16%) was one of the limitations of the present study. Further, the area of brain involvement due to stroke was not homogenous among the participants. The subjects with central
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poststroke pain syndromes64,65 such as dysesthesia, hyperalgesia, and allodynia were not included in the study. In addition to this, the level of illusion during the experimental protocol could not be measured. The strength of illusion perceived by the participant could influence the recovery at the individual level. Although MT intervention comprised sensory components such as steregnosis and vibration, specific measures for these components were not utilized. Refinement of the protocol considering variety of textures, objects, size and shape, and type/level of sensory deficit is recommended for the further studies. Moreover, investigation should also be performed at different stages of stroke. Trials with large sample, sham therapy for controls, and comparison of motor- and sensory-based MT may also be conducted.
Conclusion MT may be considered as a feasible and effective regime for enhancing cutaneous sensibility among chronic stroke survivors. The mirror illusion induced by MT may be utilized for sensory as well as motor deficits. The intervention not only acts on sensory deficit of the moreaffected hand but also on the same of the less-affected side.
Conflict of Interest None.
References 1. Bolognini N, Russo C, Edwards DJ. The sensory side of post-stroke motor rehabilitation. Restor Neurol Neurosci 2016;34:571-586. 2. Lima NM, Menegatti KC, Yu E, et al. Sensory deficits in ipsilesional upper-extremity in chronic stroke patients. Arq Neuropsiquiatr 2015;73:834-839. 3. Bowden JL, Lin GG, McNulty PA. The prevalence and magnitude of impaired cutaneous sensation across the hand in the chronic period post-stroke. PLoS One 2014;9: e104153. 4. Doyle SD, Bennett S, Dudgeon B. Upper limb post-stroke sensory impairments: the survivor's experience. Disabil Rehabil 2014;36:993-1000. 5. Doyle S, Bennett S, Fasoli SE, et al. Interventions for sensory impairment in the upper limb after stroke. Cochrane Database Syst Rev 2010;12. CD006331. 6. Kessner SS, Bingel U, Thomalla G. Somatosensory deficits after stroke: a scoping review. Top Stroke Rehabil 2016;23:136-146. 7. Campfens SF, Zandvliet SB, Meskers CG, et al. Poor motor function is associated with reduced sensory processing after stroke. Exp Brain Res 2015;233:1339-1349. 8. Scalha TB, Miyasaki E, Lima NM, et al. Correlations between motor and sensory functions in upper limb chronic hemiparetics after stroke. Arq Neuropsiquiatr 2011;69:624-629. 9. Meyer S, De Bruyn N, Lafosse C, et al. Somatosensory impairments in the upper limb poststroke: distribution and association with motor function and visuospatial neglect. Neurorehabil Neural Repair 2016;30:731-742.
ARTICLE IN PRESS 10 10. Meyer S, Karttunen AH, Thijs V, et al. How do somatosensory deficits in the arm and hand relate to upper limb impairment, activity, and participation problems after stroke? A systematic review. Phys Ther 2014;94:12201231. 11. Balci NC, Dogru E, Aytar A, et al. Comparison of upper extremity function, pain, and tactile sense between the uneffected side of hemiparetic patients and healthy subjects. J Phys Ther Sci 2016;28:1998-2001. 12. Nudo RJ, Milliken GW, Jenkins WM, et al. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 1996;16:785-807. 13. Kim JS. Pure sensory stroke. Clinical-radiological correlates of 21 cases. Stroke 1992;23:983-987. 14. Kim JS. Patterns of sensory abnormality in cortical stroke: evidence for a dichotomized sensory system. Neurology 2007;68:174-180. 15. Pumpa LU, Cahill LS, Carey LM. Somatosensory assessment and treatment after stroke: an evidence-practice gap. Aust Occup Ther J 2015;62:93-104. 16. Schabrun SM, Hillier S. Evidence for the retraining of sensation after stroke: a systematic review. Clin Rehabil 2009;23:27-39. 17. Laufer Y, Elboim-Gabyzon M. Does sensory transcutaneous electrical stimulation enhance motor recovery following a stroke? A systematic review. Neurorehabil Neural Repair 2011;25:799-809. 18. de Diego C, Puig S, Navarro X. A sensorimotor stimulation program for rehabilitation of chronic stroke patients. Restor Neurol Neurosci 2013;31:361-371. 19. Perez-Cruzado D, Merchan-Baeza JA, Gonzalez-Sanchez M, et al. Systematic review of mirror therapy compared with conventional rehabilitation in upper extremity function in stroke survivors. Aust Occup Ther J 2017;64:91-112. 20. Arya KN, Pandian S. Effect of task-based mirror therapy on motor recovery of the upper extremity in chronic stroke patients: a pilot study. Top Stroke Rehabil 2013;20:210-217. 21. Arya KN, Pandian S, Kumar D, et al. Task-based mirror therapy augmenting motor recovery in poststroke hemiparesis: a randomized controlled trial. J Stroke Cerebrovasc Dis 2015;24:1738-1748. 22. Arya KN. Underlying neural mechanisms of mirror therapy: implications for motor rehabilitation in stroke. Neurol India 2016;64:38-44. 23. Sidarta A, Vahdat S, Bernardi NF, et al. Somatic and reinforcement-based plasticity in the initial stages of human motor learning. J Neurosci 2016;36:11682-11692. 24. Enders LR, Seo NJ. Effects of sensory deficit on phalanx force deviation during power grip post stroke. J Mot Behav 2017;49:55-66. 25. Brown KE, Neva JL, Feldman SJ, et al. Sensorimotor integration in chronic stroke: baseline differences and response to sensory training. Restor Neurol Neurosci 2018;36:245-259. 26. Hakon J, Quattromani MJ, Sjolund C, et al. Multisensory stimulation improves functional recovery and restingstate functional connectivity in the mouse brain after stroke. Neuroimage Clin 2018;17:717-730. 27. Proprioception deficit in chronic stroke-Upper extremity function and daily living. Plos one 13, 2018, e0195943 28. Smania N, Montagnana B, Faccioli S, et al. Rehabilitation of somatic sensation and related deficit of motor control in patients with pure sensory stroke. Arch Phys Med Rehabil 2003;84:1692-1702.
K.N. ARYA ET AL. 29. Nudo RJ, Friel KM, Delia SW. Role of sensory deficits in motor impairments after injury to primary motor cortex. Neuropharmacology 2000;39:733-742. 30. Boutron I, Altman DG, Moher D, et al. Consort statement for randomized trials of nonpharmacologic treatments: a 2017 update and a consort extension for nonpharmacologic trial abstracts. Ann Intern Med 2017;167:40-47. 31. Snyder BA, Munter AD, Houston MN, et al. Interrater and intrarater reliability of the Semmes-Weinstein monofilament 4-2-1 stepping algorithm. Muscle Nerve 2016;53:918-924. 32. Enders LR, Hur P, Johnson MJ, et al. Remote vibrotactile noise improves light touch sensation in stroke survivors' fingertips via stochastic resonance. J Neuroeng Rehabil 2013;10:105. 33. Trombly CA. Occupational therapy for physical dysfunction. 1995 34. Kim JS, Yi SJ. Comparison of two-point discrimination perception in stroke patients with and without diabetes mellitus. J Phys Ther Sci 2013;25:1007-1009. 35. Wolny T, Linek P, Michalski P. Inter-rater reliability of two-point discrimination in acute stroke patients. NeuroRehabilitation 2017;41:127-134. 36. O'Sullivan SB, Schimtz TJ, Fulk GD. Physical rehabilitation, 6th ed. Philadelphia; 2014. 37. Pandian S, Arya KN. Stroke-related motor outcome measures: Do they quantify the neurophysiological aspects of upper extremity recovery. J Bodyw Mov Ther 2014;18:412-423. 38. Page SJ, Hade E, Persch A. Psychometrics of the wrist stability and hand mobility subscales of the Fugl-Meyer assessment in moderately impaired stroke. Phys Ther 2015;95:103-108. 39. Page SJ, Levine P, Hade E. Psychometric properties and administration of the wrist/hand subscales of the fuglmeyer assessment in minimally impaired upper extremity hemiparesis in stroke. Arch Phys Med Rehabil 2012;93:2373-2376. 40. Santisteban L, Teremetz M, Bleton JP, et al. Upper limb outcome measures used in stroke rehabilitation studies: a systematic literature review. PLoS One 2016;11:e0154792. 41. Huang CY, Lin GH, Huang YJ, et al. Improving the utility of the brunnstrom recovery stages in patients with stroke: validation and quantification. Medicine 2016;95:e4508. 42. Brunnstrom S. Motor testing procedures in hemiplegia: Based on sequential recovery stages. Phys Ther 1966;46: 357-375. 43. Pavlova EL, Borg J. Impact of tactile sensation on dexterity: a cross-sectional study of patients with impaired hand function after stroke. J Mot Behav 2018;50:134-143. 44. Carey LM, Matyas TA, Baum C. Effects of somatosensory impairment on participation after stroke. Am J Occup Ther 2018;72. 7203205100p7203205101-7203205100p7203205110. 45. Carlsson H, Gard G, Brogardh C. Upper-limb sensory impairments after stroke: self-reported experiences of daily life and rehabilitation. J Rehabil Med 2018;50:45-51. 46. Sarasso E, Agosta F, Temporiti F, et al. Brain motor functional changes after somatosensory discrimination training. Brain Imaging Behav 2018;12:1011-1021. 47. Cheng CH. Effects of observing normal and abnormal goal-directed hand movements on somatosensory cortical activation. Eur J Neurosci 2018;47:48-57. 48. Kwon HG, Jang SH, Lee MY. Effects of visual information regarding tactile stimulation on the somatosensory cortical activation: a functional MRI study. Neural Regen Res 2017;12:1119-1123.
ARTICLE IN PRESS MIRROR ILLUSION FOR SENSORI-MOTOR TRAINING IN STROKE 49. Saleh S, Adamovich SV, Tunik E. Mirrored feedback in chronic stroke: recruitment and effective connectivity of ipsilesional sensorimotor networks. Neurorehabil Neural Repair 2014;28:344-354. 50. Fritzsch C, Wang J, Dos Santos LF, et al. Different effects of the mirror illusion on motor and somatosensory processing. Restor Neurol Neurosci 2014;32:269-280. 51. Pandian JD, Arora R, Kaur P, et al. Mirror therapy in unilateral neglect after stroke (must trial): a randomized controlled trial. Neurology 2014;83:1012-1017. 52. Tosi G, Romano D, Maravita A. Mirror box training in hemiplegic stroke patients affects body representation. Front Hum Neurosci 2017;11:617. 53. Wu CY, Huang PC, Chen YT, et al. Effects of mirror therapy on motor and sensory recovery in chronic stroke: a randomized controlled trial. Arch Phys Med Rehabil 2013;94:1023-1030. 54. Winward CE, Halligan PW, Wade DT. Somatosensory recovery: a longitudinal study of the first 6 months after unilateral stroke. Disabil Rehabil 2007;29:293-299. 55. Meyer S, De Bruyn N, Krumlinde-Sundholm L, et al. Associations between sensorimotor impairments in the upper limb at 1 week and 6 months after stroke. J Neurol Phys Ther 2016;40:186-195. 56. Winstein C. The attend trial: an alternative explanation with implications for future recovery and rehabilitation clinical trials. Int J Stroke 2018;13:112-16.1. 57. Arya KN, Pandian S, Kumar D. Task-based mirror therapy enhances ipsilesional motor functions in
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Mirror Illusion for Sensori-Motor Training in Stroke: A Randomized Controlled Trial Kamal Narayan Arya, MOT, PhD,* Shanta Pandian, MOT,* Vikas, BOT,* and Vinod Puri, DM† Background: Poststroke, sensory deficits are not uncommon. In spite of the close association between the sensory and motor recovery, the deficits are usually underemphasized. Mirror therapy (MT), a neural-based approach for the motor deficit has not been explored for the sensory impairment. The objective of the present study was to develop and determine the effect of a MT program for sensori-motor impairment among poststroke subjects. Methods Design: Randomized controlled trial. Setting: Functional therapy laboratory of Rehabilitation Institute. Participants: Thirtyone chronic poststroke subjects (17 experimental and 14 controls), aged between 30 and 60 years, with diminished light touch in the hand. Outcome Measure: Semmes Weinstein Monofilament (cutaneous threshold), 2-Point discrimination test (touch discrimination) and Fugl-Meyer Assessment (hand motor recovery). Intervention: The experimental group received sensory stimulus such as tactile perception and motor tasks on the less-affected hand using mirror box. The control counterparts underwent only dose-matched conventional program. 30 sessions with a frequency of 5/week were imparted to the groups. Results: Post intervention, there was a significant (P < .004) increase up to 30% positive touch-response for the hand quadrants among the experimental group in comparison to only 13.5% rise for the same among the controls. The cutaneous threshold of the less-affected palm also improved significantly among the experimental subjects in comparison to the controls (P = .04). Conclusion: MT may be considered as a promising regime for enhancing cutaneous sensibility in stroke. The mirror illusion induced by MT may be utilized for sensory and motor deficits as well as for the more-affected and less-affected hands. Key Words: Cerebrovascular accident—Cutaneous threshold—Hand— Monofilament—Rehabilitation—Tactile—2-point discrimination © 2018 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction Sensory impairment is not uncommon after stroke; however usually not emphasized due to the apparent motor paresis.1 The somatosensory deficits are not only From the *Pandit Deendayal Upadhyaya National Institute for Persons with Physical Disabilities, New Delhi, India; and †Department of Neurology, GB Pant Post Graduate Institute of Medical Education and Research, New Delhi, India. Received May 16, 2018; revision received June 27, 2018; accepted July 5, 2018. Financial disclosure: Indian Council of Medical Research, 5/4-5/2/ ADR/2014-NCD-I, New Delhi, India for financial assistance. Address correspondence to Kamal Narayan Arya, MOT, PhD, Pandit Deendayal Upadhyaya National Institute for Persons with Physical Disabilities, New Delhi, India. E-mail: [email protected] 1052-3057/$ - see front matter © 2018 National Stroke Association. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jstrokecerebrovasdis.2018.07.012
presented on the contralateral body side to the brain lesion but also on the ipsilateral side.2 The sensory recovery has been found to be strongly associated with the level of the motor recovery.3 Further, the sensory deficit affects quality of life among stroke subjects.4 Up to 85% of the subjects could experience sensory deficits. The individual may exhibit deficit in tactile, propriopception, vibration, steregnosis, and 2-point discrimination abilities.5,6 The sensory deficits hamper the ability to utilize the available motor level in the functional tasks.7 Thus, adequate motor recovery depends upon the intact sensation.8-10 The impaired sensation along with the complex motor deficits increases the disability manifold.6,11 In a lesioned brain, the motor control is facilitated by alternative sensorimotor pathways recruited from secondary motor areas. Poststroke sensory deficits are the consequence of structural damage of cortical and subcortical structures. The primary somatosensory area situated in
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the postcentral gyrus is commonly affected regions.6,12 Thalamus and basal ganglia are the most crucial areas which coordinate sensory information with motor cortex. Usually, thalamic stroke is supposed to be sensory stroke; whereas clinically a diversity of sensory loss presentation has been observed among other lesions also.13,14 The identification and assessment of sensory issues in poststroke subjects are still under explored. The apparent motor impairment in contrast to the subtle sensory deficits could be the reason for overlooking the issue. Additionally, stroke specific sensory outcome measures are sparsely available.6,15 In poststroke, sensory training of varied range has been investigated.5,6,16 The techniques may range from passive techniques such as somatosensory electrical stimulation to active retraining of stereognosis, proprioception, discriminating, and localizing sensations.16,17 The other investigated sensory interventions are sensory electrical stimulation, thermal stimulation, and pneumatic compression technique. However, none of them exhibited sufficient evidence for their effectiveness.5,6 Further, sensory and motor techniques have also been combined to explore the response of upper limb function. It has been suggested to amalgamate the techniques to enhance the upper limb recovery.18 Techniques such as mirror Therapy (MT) have been developed for motor rehabilitation in stroke.19 MT provides a form of visual illusion by watching the reflection of the unaffected limb on a mirror. The patient performs movement of the unaffected limb and creates an image of the affected limb in a mirror.20,21 The illusion enhances the interhemispheric communication as well as activity of the certain brain areas associated with the motor performance of the affected limb. Various mechanisms have been proposed to be responsible for MT including mirror neuron system.22 MT using tasks has been proven to be an effective technique for the upper limb rehabilitation among stroke patients.20-22 Although activity or task-based MT unquestionably utilize sensations to complete the task, the technique has not been explored for sensory rehabilitation. It is evident that sensory and motor functions are interlinked in healthy and lesioned brain.23,24 Integration of sensory abilities is crucial for the recovery of motor control and motor learning.1,25,26 However, the sensory intervention has been underemphasized due to motor rehabilitation.1 Poststroke, both the functions gets impaired and recovered together.4,5,27-29 However, till today, all the stroke rehabilitation methods have developed exclusively for the motor aspect. A novel treatment training to treat sensory and motor impairments needs to be developed. The objective of study was to develop a MT program using tasks for sensory and motor impairment and to determine the effect of the protocol on sensory and motor recovery among poststroke survivors.
Methods The present study followed the CONSORT (Consolidated Standards of Reporting Trials) guidelines for the nonpharmacologic treatments.30 The protocol of the study was approved by the Institutional Ethics Committee of Pandit Deendayal Upadhyaya National Institute for Persons with Physical Disabilities. The informed signed consent was obtained from all the enrolled participants. The potential subjects were recruited from a nationallevel rehabilitation institute situated in an urban city. The investigation was conducted in a functional therapy laboratory of the institute. The participants were enrolled in the study if they met the following inclusion criteria: (i) unilateral stroke of >6 months, (ii) hemiparesis of right or left side, (iii) age between 30 and 60 years, and (iv) sensory deficit in the palamar aspect of the hand and fingers (assessed by the Semmes-Weinstein monofilaments as diminished light touch).24,31 However, the subjects were excluded if they exhibited any of the following: (i) cognitive and perceptual deficits (determined clinically by trail making test, digit span, copying and drawing, line-bisection, and functional performance), (ii) receptive communicative disorder, (iii) contracture of hand muscles or any fixed wrist/hand/finger deformity, (iv) complex regional pain syndrome, (v) diabetic or any other type of neuropathy, and (vi) skin disorder affecting the upper limb. The study was a randomized controlled, assessor blinded trial. Sample size was not calculated for the study as no MT study was found using sensory measure as a primary outcome. The subjects were not blinded due to nature of the intervention. The selected subjects were randomly divided into the experimental and control group using computer generated random numbers. The randomization procedure was performed by a research assistant who was not concerned with the present study. The allocation of intervention was divided in the ratio of 1:1 and that was serially arranged in sealed opaque paper envelopes. After getting signed written informed consent, the subjects were enrolled for the study. The experimental group subjects received 30 sessions, 40 minutes each across the 6 weeks (5/week). Additionally, 50 minute conventional occupational therapy was also provided. The rationale for providing the conventional therapy to the experimental group was to avoid deprivation of the affected upper limb from the motor and sensory training. The control group subject received only standard motor and sensory rehabilitation; however, for 90 minutes duration to match the total dosage of therapy between the groups. Specifically, the experimental participants received task-based mirror therapy using the mirror frames or mirror box (dimensions and purpose are provided in the Box 1). The mirrored wall of the frame/box was placed vertically along the midsternum level. The affected limb was hidden beside the nonreflective side of the wall. The subjects were provided sensory stimulus (various textures, size, and
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Box 1. Type of mirror
Dimension
Purpose
Short mirror frame (Table mounted) Mirror box (Wooden)
18 £ 16 inches
Used for sensory intervention, as both the sides are free to provide sensory stimulus Used for the wrist and hand movements
24 £ 18 £ 14 inches
Box 2. Sensation
Intervention
Light touch Vibration
Piece of cotton/tissue paper were lightly touched or stroked on the all quadrants of hands. Electrical motorized toothbrush was used to provide stimulation from the fingers to palm in distal to proximal pattern. Blunt end of a pen was touched at the different points on the hands
Tactile localization Stereognosis Recognition of texture
Recognition and manipulations of various familiar objects. Hard to soft material was used in order (scrubber, steel wool, metal, washing brush, denim cloth, wool, cotton ball).
shape) on the less-affected and the affected hands simultaneously to induce mirror illusion for sensory perception (Box 2) (Fig 1). The stimulus was provided in 2 ways: selfperception and passively applied by the therapist. The self-perception of the stimulus was performed bilaterally by the higher motor stage subjects else unilaterally by the less-affected side. For stereognosis, object recognition was performed without vision occlusion. Each sensory stimulus was imparted for 2-5 minutes to a total of 20 minutes. The participants were also provided need-based auditory feedback and stabilization of the paretic limb (by another therapist). The practice of paretic wrist and hand using various tasks were also conducted as MT (Box 3). The motor tasks were selected as per the specific impaired items of Fugl-Meyer assessment (wrist-hand). Simultaneous bilateral movements (more-affected hand without task) were preferred; however, for lower motor stage
subjects only unilateral performances were allowed. The movements were provided in repetition of 20-50 to a total of 20 minutes. Sensory stimuli of similar sensations on the affected hand and neurophysiological based motor rehabilitation were also imparted as conventional therapy.
Primary Outcome Measures Semmes Weinstein Monofilament Semmes-Weinstein monofilaments (SWM) are precisely calibrated nylon filaments used to measure diminished cutaneous sensation. The monofilament sets ranged from normal, diminished light touch, diminished protective sensation, and loss of protective sensation.31 The monofilament test has been used in other stroke studies to measure the sensory deficits.24,32 In the present study, to have
Figure 1. The left hemiparetic subject receiving sensory stimulus (rough texture) simultaneously on both the sides using mirror frame. The illusion of right hand has been created which is perceived as the left hand.
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Box 3. S. No.
Movement
Activity
1. 2. 3. 4. 5. 6. 7. 8.
Wrist Wrist Wrist Wrist Fingers Fingers Fingers Fingers
Dorsiflexion 0-30˚ using cylindrical block Stability at 15˚; holding soft ball Repeated dorsiflexion / palmar flexion using cylindrical block Circumduction; making a circle by pen Flexion/extension; ball squeezing Clay activity (kneading) Clay activity (making balls) Zymkit activity
a comprehensive sensory status, the assessment was conducted on the entire hand (palmar aspect) by dividing it into the 30 quadrants (Fig 2).33 The filaments were applied on each quadrant to score the positive response for the most sensitive to crude filaments, cutaneous threshold force ranging from .0045 to 447 g (.0045-.0677 g=normal sensation, .1660-.4082 g=diminished light touch, .69582.0520 g=diminished protective sensation, 3.632-447 g=loss of protective sensation).
2-Point Discrimination The static 2-point discrimination (2PD) test was applied using the modified vernier caliper with blunted extension. The scoring is done in mm based on the ability to perceive the 2 points being touched simultaneously. The testing was conducted on all the 30 quadrants of hand. The normal scores were considered as 3 mm, 4-5 mm, 6-7 mm, and 710 mm, respectively for the distal phalanx, middle phalanx, proximal phalanx, and palm.33 The test has been found to be a reliable measure and used in poststroke subjects.34,35 Both SMF and 2PD were also measured on the lessaffected hand for the additional reference value. In addition to above measures, the other somato-sensory abilities such as pain, temperature, stereognosis were assessed clinically as a part of standard rehabilitation assessment.33,36
Secondary Outcome Measure Fugl-Meyer Assessment (FMA) Fugl-Meyer's assessment (FMA) assesses the poststroke motor recovery in a hierarchically organized pattern. The motor items primarily comprise reflexive, synergistic, outof-synergy, movements. The 33-item upper extremity section is scored on 3-point ordinal scale ranging from 0 (no performance) to 2 (faultless performance) with a maximum score of 66. The section further has 2 components; upper arm and wrist-hand (FMA-WH) with sub score of 36 and 30, respectively. FMA has been widely used in poststroke studies since decades and found to be a reliable and valid measure.37-40 Subsection FMA-WH has been used in the present study.
Data Analysis The data analysis was performed using IBM SPPS version 23. The analysis of covariance (ANCOVA) was carried out to determine the difference between the experimental and control groups for the SWM and FMA measures. The median score for each finger/palm unit were considered for mean calculation of the sample. Since the maximum cutaneous force threshold measured by SWM was 447 g, the score of 448 g was awarded for the
Figure 2. Sensory assessment of the right paretic hand using Semmes Weinstein Monofilamens on 30 testing quadrants mapped on hands.
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Figure 3. Flow chart of the study.
quadrants responded not even to the crudest filament. Further, the number of positive responses for each cutaneous threshold force as assessed by the SWM was calculated to assess the pre and post intervention changes. The total positive response respectively for the palm and finger were 238 (17 subject £ 14 finger quadrant) and 272 (17 subject £ 16 palm quadrant) among the experimental subjects whereas 196 (14 subject £ 14 finger quadrant) and 224 (14 subject £ 16 palm quadrant) in the control group. Chi-square test was used to compare the responses between the groups. The median value for the finger (14 quadrants)/palm (16 quadrants) for each participant was considered for the analysis of the 2PD measures. The conventional value of P < .05 was considered as the level of significance.
Results Eighty-nine subjects were screened for the enrollment out of which 58 either did not meet the eligibility criteria or did not agree to participate in the study. Thirty-one participants were randomly divided into the experimental (n = 17) and control (n = 14) groups. Figure 3 shows the flow of participants throughout the study. One control subject discontinued the intervention after few sessions and an experimental subject did not report for the post assessment. All other subjects completed the protocol of the study. The average age of the study participants was 46 years with 26(84%) males. The mean post stroke duration was 15 months with 14(45%) subjects with ischemic stroke. Seventeen (55%) and 14 (45%) subjects were at
Brunnstrom recovery stage41,42 3 and 4, respectively. The other demographic details of the participants are mentioned in the Table 1. MT based sensory training was found to be feasible among all the participants. No adverse event was reported by any of the subjects. The average cutaneous threshold on the less-affected fingers and palm were .136 g (SD .111) and .457 g (SD .362), respectively for the experimental subjects whereas the same for the controls were .262 g (SD .219) and .457 g (SD .388), respectively. The mean cutaneous threshold on the affected fingers and palm were 346.08 g (SD 189.52) and 346.58 g (SD 188.39), respectively for the experimental group. The same for the controls were 357.37 g (SD 180.88) and 357.43 g (SD 180.65), respectively. The threshold on the less-affected side (fingers .193; SD .177 and palm .457; SD .368) of all participants was significantly (P < . 001) lower than that on the affected side (fingers 351.18; SD 182.66 and palm 351.48; SD 181.94). Post intervention, the less-affected fingers of the experimental demonstrated same threshold whereas the palm exhibited the threshold of .442 g (SD .372). The change of palm was significantly (P = .04; 95% CI .008.0303) better than that of the control group (.598 g SD .552). The less-affected fingers of the control showed the threshold of .279 g (SD .225). The mean change in cutaneous threshold for the affected fingers and palm among the experimental subject were not found to be significant in comparison to that of the controls. Table 2a shows the pre and post mean changes for the SWM of the affected fingers and palm between the
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Table 1. Demographic and clinical characteristics of the participants S. No. 1. 2. 3. 4. 5.
6. 7. 8.
9.
10. 11. 12. 13. 14. 15.
Characteristic
Experimental group (n = 17)
Control group (n = 14)
Test statistics
Age (years) Mean § SD Time since stroke (months) Mean § SD Male/female (%) Socio-economic status (BPL/ LIG/MIG/HIG) Educational qualification (10th/12th/UG/PG) (%)
44.12 § 9.08 13.35 § 10.12
47.93 § 9.10 17.00 § 13.28
t:p = .191 t:p = .393
13(76.5%)/04(23.5%) 00(00%)/11 (65%)/6/(35%)/00(00%)
13(93%)/01(07%) 2(14%)/3(21%)/6(43%)/3(21%)
x2:p = .344
09(53%)/
05(36%)/
—
02(12%)/ 04(23.5%)/ 02(12%)/ 13(76.5%)/4(23.5%)
02(14%)/ 02(14%)/ 05(36%)/ 14(100%)/00(00%)
—
08(47%)/9(53%) 00(00%)/
6(43%)/08(57%) 00(00%)/
06(35%) / 01(6%) / 09(53%)/ 01(6%)
07(50%)/ 02(14%)/ 05(36%)/ 00(00%)
00(00%) 13(76.5%) 02(12%) 00(00%) 02 (12%) 02(12%) 9(53%)/8(47%)
00(00%) 14(100%) 02(14%) 02(14%) 05(36%) 00(00%) 9(64%)/5(36%)
— — x2:p = 1 — x2:p = .198 — x2:p = .717
17(100%)/0(0%)
14(100%)/0(0%)
—
2(12%)/6(35%) /4(23.5%) /5(29%) 6(35%)/4(23.5%)/4(23.5%) /3(18%) 10(59%) 00(00%)
6(43%)/3(21%)/3(21%)/2(14%) 9(64%)/3(21%)/0 (00%)/2(14%) 9(64%) 02(14%)
— — x2:p = .756 —
Marital status (married/ unmarried) Ischemic/Hemorrhagic (%) Area of involvement (Frontoparietal/basal ganglia/thalamus/multiple/others)
Risk factors Hereditary Hypertensive Chronic smokers Alcoholic Diabetes mellitus Obesity Side of involvement (Right/ left) (%) Dominant side (Right/left) (%) BRS-U (Stage 2/3/4/5) BRS-H (Stage 2/3/4/5) Shoulder support Hand splint
—
x2:p = .815 —
BPL, below poverty line; BRS- H, Brunnstrom recovery stage of hand; BRS-U, Brunnstrom recovery stage of arm; HIG, higher income group; LIG, lower income group; MIG, middle income group; PG, post graduate; SD, Standard deviation; UG, under graduate.
Table 2a. Pre- and postintervention changes on outcome measure among experimental and control groups Outcome measure
Pre-intervention
Difference between the means (95% CI)
F
P value
346.08 § 189.52 357.37 § 180.88 345.78 § 189.35 357.23 § 180.80
.068
.991
346.58 § 188.39 357.43 § 180.65 317.08 § 182.78 357.29 § 180.57
2.92
.098
Experimental group (n = 17)
SWM- Affected Fingers (Mean § SD) in g SWM- Affected Palm (Mean § SD) in g FMA-WH (Mean § SD)
Post-intervention
12.12 § 11.14
Control group (n = 14)
15.14 § 10.61
Experimental group (n = 17)
16.18 § 10.62
Control group (n = 14)
16.13 § 10.59
1.64¡4.23 6.01 <.001
CI, confidence interval; F, test value for ANCOVA; FMA-WH, Fugl-Meyer Assessment (Wrist-Hand); n, number; SD, standard deviation; SWM, Semmes-Weinstein monofilaments.
ARTICLE IN PRESS MIRROR ILLUSION FOR SENSORI-MOTOR TRAINING IN STROKE
groups. The detail about the number of positive (447 g)/no response (>448 g) for pre and post intervention for the total quadrants among the experimental and control groups is mentioned in the Table 2b. Post intervention, there was a significant (P = .004) increase of 27% positive responses for the finger quadrants among the experimental group in comparison to only 13.5% rise for the same among the controls. Similarly, the positive response for the palm increased significantly (P = .0001) by 30% in the experimental group whereas the same was only 14% among the controls. Only 8 (26%) subjects (4; 23.5% experimental and 4; 28.5% controls) responded to the 2PD testing on the affected side. The average 2PD in the finger and palm were 4.35 mm and 12.78 mm, respectively in the experimental group whereas 4.7 mm and 10.77 mm, respectively among the controls. Post intervention, there was increase of 3 (18%) subjects in the experimental group that could respond to 2PD test among the experimental group. All the subjects responded to the 2PD test on the lessaffected side. Both the groups exhibited average 2PD of 3.5 mm and 7 mm, respectively in the finger and palm. Further, after intervention the motor scores on FMAWH significantly (P < . 001) enhanced to 16.18 (SD 10.62) from 12.12 (SD 11.14) among the experimental subjects in comparison to the controls (16.13; SD 10.59 from 15.14; SD 10.61) (Table 2a).
Discussion Sensory ability is vital for an efficient motor performance. The hand sensibility is strongly related to the dexterous performance.43 The poor hand sensation also affects the motor control. In spite of the same level of motor paresis, the stroke subjects with sensory deficit are unable to induce appropriate force to avoid dropping of the object from the hand.24 The sensory impairment is also associated with the restriction in the participation resulting into a negative impact on daily life among post stroke survivors.44,45 Further, sensory training has neural basis, the therapy may induce cortical reorganization. In healthy individuals, sensory training led to the lateralization of sensory-motor cortical activity during task performance.46 MT may be considered as a promising technique in stroke rehabilitation. The present study demonstrated favorable changes in terms of number of the affected hand quadrants in response to MT. The technique allowed poststroke subject to experience normal sensory-motor perception of the paretic upper limb. The observation of normal hand movement may augment the strength of functional connectivity within the somatosensory cortex.47 The tactile inputs along with the visual feedback induce bilateral activation of primary sensory-motor cortex and secondary somatosensory cortex.48 The networking between the sensory and motor cortex also gets
7
enhanced in response to MT.49 Also, MT based movements lead to immediate activation of the somatosensory cortex in comparison to the motor area.50 This could be the possible neural mechanism elucidating the effect of regime in the present study. In addition to this, the average cutaneous threshold on the affected hand of the experimental subject did not improve in comparison to the controls. This could be due to the severity of sensorymotor deficit among the participants. The subjects achieved cutaneous sensibility in some of the hand quadrants not all. On estimating the average of all the quadrants, the change in the threshold was found to be negligible. To our knowledge, this was the first study in which the sensory assessment was performed on the 30 hand segments. The minute evaluation explored the real extent of impairment as well as the pattern of recovery. The participants had low motor level and high sensory deficit. The low motor level has been found to be associated with the low cutaneous sensibility. However, the poor sensation may also be observed among mild paretic subjects.3 In the present study, 3 subjects with mild paresis had severely impaired sensations. MT technique has been explored and found to evident for motor and perceptual deficits.19,51,52 Exclusively sensory based MT in stroke has been sparsely explored. Although in a study,53 the effect of MT was evaluated for the sensory recovery; the intervention protocol was purely motor-based. The regime enhanced the sensory ability among the participants included on the basis of motor impairment only. The sensory impairment among chronic stroke subjects is evident. The subject with poor motor abilities experience more sensory deficit in comparison to those with the good control.3 However, the pattern of sensory recovery among acute or chronic stroke is conflicting.54 Further, the sensory recovery is related to the motor and functional recoveries.9,10,55 The association of sensory deficit and motor or functional outcome may increase with the chronicity.55 In the present study, the limited positive changes for the cutaneous threshold on the affected hand after the intervention could also be attributed to the intricate aspect of stroke rehabilitation.56 Since the subjects achieve positive changes on the certain hand quadrants rather than on the entire affected hand and had no goal regarding the target sensitivity, the success of the regime from the patient's perspective is questionable. In the present study, the less-affected side also exhibited sensory recovery after the experimental intervention. However, the control subjects did not receive any sensory stimulation on the less-affected side. The utilization of the less-affected side is the integral component of MT. The sensory stimulation to induce illusion for the affected side also provoked sensations on the less-affected side. The sensory issues such as tactile deficit on the less-affected side are also evident in the literature.2,11 MT has also been
8
Table 2b. Cutaneous threshold (number of positive responses) pre and post intervention among the experimental and control groups Cutaneous threshold (g)
Preintervention: Fingers (14 quadrants) Experimental Control group group (n = 17) (n = 14) Total response- Total response17 £ 14 = 238 14 £ 14 = 196 150 46
0 0 0 8 20 0 0 0 0 2 0 0 6 12 8 0 0 0 0 0
4 3 0 4 3 0 0 0 1 1 2 1 3 2 0 12 10 0 0 0
x2:p = .988
116 122
123 73
36 15 0 8 20 0 3 3 0 2 0 0 8 10 8 0 9 0 0 0
4 3 1 20 13 0 0 0 1 1 2 0 0 0 0 16 12 0 0 0
Test statistics
x2:p = .004*
Experimental group (n = 17)
Control group (n = 14) Total response- Total response17 £ 16 = 272 14 £ 16 = 224 190 82
168 56
18 0 10 16 6 0 0 0 20 12 0 0 0 0 0 0 0 0 0 0
5 8 1 3 0 0 0 1 2 0 8 1 13 2 4 8 0 0 0 0
Test statistics
x2:p = .241
Postintervention: Palm (16 quadrants) Experimental Control group group (n = 17) (n = 14) Total response- Total response17 £ 16 = 272 14 £ 16 = 224 110 162
136 88
42 37 12 19 20 0 0 0 20 12 0 0 0 0 0 0 0 0 0 0
4 8 2 15 20 0 0 1 2 0 8 3 11 2 5 7 0 0 0 0
Test statistics
ARTICLE IN PRESS
*Significant † Highly significant
182 56
Experimental Control group group (n = 17) (n = 14) Total response- Total response17 £ 14 = 238 14 £ 14 = 196
Preintervention: Palm (16 quadrants)
x2:p = .0001y
K.N. ARYA ET AL.
>447 447 Distribution of responses 447 g 447.0 281.5 127.0 75.00 29.00 15.00 11.70 8.65 5.50 3.632 2.0520 1.4940 1.1940 .6958 .4082 .1660 .0677 .0275 .0230 .0045
Test statistics
Postintervention: Fingers (14 quadrants)
ARTICLE IN PRESS MIRROR ILLUSION FOR SENSORI-MOTOR TRAINING IN STROKE
found to effective in enhancing the subtle motor impairment on the less-affected side.57 Furthermore, no evident protocol has been found for the management of the ipselesional sensory impairment. The discrimination ability, affecting hand function is not uncommon among the stroke subjects.58,59 In the present study, only few (26%) participants could respond to 2PD test; thus, the effect of intervention could not be analyzed. However, the range of 2-PD these participants could be utilized as reference value for further investigation. The experimental intervention also enhanced the motor recovery of the hand. Even short duration sensory intervention had a favorable implication on motor recovery. In a randomized cross-over trial, immediately after sensory stimulation such as vibration positive change on the hand function and reaching ability was observed.60 However, in a recent systematic review, there is a weak evidence for the sensory training facilitating the motor outcome.61 It is worthwhile to mention that the mechanism of MT is unique than the techniques used in the previous investigation. Although there are numerous sensory assessment tools in practice, no stroke specific sensory outcome is available. Scales such as Erasmus MC modification to the Nottingham Sensory Assessment has been recommended for the neurological conditions.62 However, the scale comprises the items for the entire body part not the specific hand segment.63 Considering the functional implication, a sensory measure should explore the hand evaluation in detail. Further, in the present study, SWM could only provide the measurement for the cutaneous threshold up to 447 g. The subjects who did not respond to the maximum force were awarded the score of 448 g for the purpose of analysis. The number of such responses was substantial that lead to the limited use of SWM. This further explains the less favorable results for the average change of SWM between the groups. Similarly 2PD has limited application in the present study; about 1/4th of the subjects could response to the test. The discrimination ability in the hand/fingers of the majority of the subjects was absent. Since 2PD test is scored as the minimum distance between the touch stimuli, it does not have any scoring provision for the absence of the discrimination ability. Thus, ANCOVA was not utilized for the 2PD analysis. Sensory assessment and management is considered to be vital by the practitioners. However, the evidence-based clinical application is sparse in stroke rehabilitation.15 The present study provides a novel method of sensory intervention not only for the more-affected hand but also for the less-affected side. Additionally, MT, a versatile method simultaneously acts on the motor deficit. The negligible number of female subjects (16%) was one of the limitations of the present study. Further, the area of brain involvement due to stroke was not homogenous among the participants. The subjects with central
9
poststroke pain syndromes64,65 such as dysesthesia, hyperalgesia, and allodynia were not included in the study. In addition to this, the level of illusion during the experimental protocol could not be measured. The strength of illusion perceived by the participant could influence the recovery at the individual level. Although MT intervention comprised sensory components such as steregnosis and vibration, specific measures for these components were not utilized. Refinement of the protocol considering variety of textures, objects, size and shape, and type/level of sensory deficit is recommended for the further studies. Moreover, investigation should also be performed at different stages of stroke. Trials with large sample, sham therapy for controls, and comparison of motor- and sensory-based MT may also be conducted.
Conclusion MT may be considered as a feasible and effective regime for enhancing cutaneous sensibility among chronic stroke survivors. The mirror illusion induced by MT may be utilized for sensory as well as motor deficits. The intervention not only acts on sensory deficit of the moreaffected hand but also on the same of the less-affected side.
Conflict of Interest None.
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