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Immediate effects of somatosensory stimulation on hand function in patients with poststroke hemiparesis: a randomized cross-over trial

Sim, Sun-Mia; Oh, Duck-Wonc; Chon, Seung-chulb

International Journal of Rehabilitation Research: December 2015 - Volume 38 - Issue 4 - p 306–312
doi: 10.1097/MRR.0000000000000126
Original articles

This study aimed to determine the immediate effects of somatosensory stimulation on hand function in patients with poststroke hemiparesis. Eleven patients with poststroke hemiparesis participated in this study. Four types (no stimulation, vibration, and light and rough touches) of somatosensory stimulation were performed randomly for 4 days applying only one type of somatosensory stimulation each day. The box and block test (BBT), the Jebsen–Taylor hand function test (JTHFT), hand grip strength (HGS), and movement distance and peak velocity of the wrist joint during a forward-reaching task were measured. The BBT and JTHFT scores for no stimulation [BBT: median (interquartile range), 0.00 (−1.00 to 1.00) and JTHFT: 2.57 (−0.47 to 4.92)] were significantly different from those for vibration [BBT: 3.00 (2.00–5.00) and JTHFT: −16.02 (−23.06 to −4.31)], light touch [BBT: 3.00 (1.00–4.00) and JTHFT: −5.00 (−21.20 to −0.94)], and rough touch [BBT: 2.00 (1.00–4.00) and JTHFT: −6.19 (−18.22 to −3.70)]. The JTHFT score was significantly higher for vibration than that for rough touch (P<0.05). The increase in HGS was significantly greater for light touch than that for no stimulation (P<0.05) and for vibration than that for light touch (P<0.05). There were significant differences for the sagittal and coronal planes in movement distance and for the sagittal and horizontal planes in peak velocity during the forward-reaching task (P<0.05). The findings suggest that somatosensory stimulation may be advantageous to improve the hand function of patients with poststroke hemiparesis, with more favorable effects observed in vibration stimulation.

aDepartment of Physical Therapy, Yuseong Wellness Hospital

bDepartment of Physical Therapy, College of Medical Science, Konyang University, Daejeon

cDepartment of Physical Therapy, College of Health Science, Cheongju University, Cheongju and Republic of Korea

Correspondence to Duck-Won Oh, PhD, Department of Physical Therapy, College of Health Science, Cheongju University, 298, Daesung-ro, Sandang-gu, Cheongju 360-764, Republic of Korea Tel: +82 43 229 8679; fax: +82 43 229 8969; e-mail: odduck@cju.ac.kr

Received March 2, 2015

Accepted June 29, 2015

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Introduction

The majority of patients with poststroke hemiparesis experience sensory and motor deficits in their upper limb, and the functional recovery of the impaired upper limb is often poor. In addition, the flexor synergy pattern of the upper limb during the recovery process of motor function after a stroke contributes toward making the performance of daily routine activities more difficult by impeding the extension movement required for the activities (Seo et al., 2010). In general, functional impairments appear more significant in the distal region of the upper limb; therefore, patients prefer to use the unaffected upper limb during daily routine activities. Preferred use of the unaffected side decreases the involvement of the affected side in functional activities, thereby causing further loss in sensory–motor function of the affected upper limb (Carr and Shepherd, 1998).

Traditionally, the application of somatosensory stimulation, including touch, pressure, temperature, and vibration, has been recognized as a beneficial therapeutic choice for functional improvement of poststroke hemiparesis in the clinical setting (Rood, 1954) because its involvement in the treatment process provides a specific opportunity to either facilitate or inhibit muscle tonus and subsequently improve motor control during functional movement. Sensory perception in the hands is an important element to perform functional movements efficiently and is fundamental to the learning process by discovering and manipulating the objects, communicating with them, and finally accepting and delivering a sense of expression. Therefore, hand function considerably influences return to a premorbid life and enhances the quality of life by accepting direct contact with objects and another individual’s body while performing purposeful tasks in the real world (Pouydebat et al., 2014).

Somatosensory cues provide the first opportunity to generate a precise movement pattern and execute appropriate motor control as an integral means of exploring intrinsic environmental properties (Jeannerod et al., 1995); however, somatosensory deficits are common after stroke, with 7–53% impairment in tactile sensation and 34–64% impairment in proprioception (Connell et al., 2008). In stroke patients with sensory deficit, regaining functional skills may be related to improvement of the motor control mechanism (Scalha et al., 2011); therefore, it is necessary to reinforce the sensory–motor control system for regulating action performance properly in spatiotemporal patterns. Somatosensory information arising from peripheral receptors is necessary for the successful execution of voluntary movements and skill acquisition; however, severe dysfunction works as a limiting factor to reduce the level of performance of daily tasks such as grasping a pen, writing, and fastening buttons during dressing (Sesto et al., 2003). Given that sensory recovery is needed to effectively perform delicate movement, somatosensory stimulation should be a priority for stroke rehabilitation (Rothwell et al., 1982).

In general, somatosensory stimulation has been shown to be useful for overcoming the learned nonuse of the affected upper limb and improving functional recovery (Doucet and Griffin, 2013). Previous studies have reported the functional benefits of somatosensory stimulation using warm and cold agents (Kawahira et al., 2010), tactile objects (Overvliet et al., 2011), and a vibration device (Conrad et al., 2011). Also, a neuroscientific study supported the use of repeated somatosensory stimulation to facilitate neural plasticity and cortical reorganization (Kalisch et al., 2010), and an EMG study found that the effects of somatosensory stimulation reduce the physiological latency in muscle contraction and increases muscle activity (Chen et al., 2010).

To our knowledge, the therapeutic effects of somatosensory stimulation in stroke patients have been studied previously (Chen et al., 2010; Kalisch et al., 2010; Overvliet et al., 2011); however, the clinical efficacy of different stimulation modes has not been definitively recognized, despite the therapeutic benefits of recovering sensory–motor function and clinical advantages such as easy application. Further, there was no attempt to find a more favorable type of somatosensory stimulation to facilitate functional performance after stroke. Accordingly, this study aimed to report the immediate effects of a single dose of somatosensory stimulation on hand dexterity and function and hand grip strength (HGS) of patients with poststroke hemiparesis as well as to determine a more favorable type of somatosensory stimulation by comparing different stimuli.

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Methods

Participants

Eleven chronic stroke patients [sex (male/female): 7/4; average age: 60.36±12.39 years; affected side (right/left): 6/5; average onset duration: 12.64±11.02; and stroke type (hemorrhage/infarction): 6/5] volunteered to participate in the present study. The inclusion criteria were as follows: (a) onset duration more than 6 months, (b) no cognitive impairment (Mini-Mental State Examination score>24 points) (Folstein et al., 1975), (c) an ability to move the upper limb of the affected side voluntarily (Brunnstrom stage<4) (Michielsen et al., 2011) with a spasticity of a lower grade (Modified Ashworth Scale<2 grades) in the upper limb of the affected side, (d) an ability to perceive and discriminate tactile stimulation, and (e) no lower motor neuron disease and orthopedic problems that would impede the study procedure and outcome. At the initiation of the study, 26 patients were recruited; however, 12 patients did not fulfill the inclusion criteria and three patients were excluded from the final data analysis because they did not participate in the entire study procedure. Before the beginning of the study, all patients were provided a detailed description of the study procedure and safety, and signed a written consent form. The current study received approval from the Institutional Review Board of Cheongju University. Table 1 shows the general characteristics of the patients and Fig. 1 summarizes the study procedure.

Table 1

Table 1

Fig. 1

Fig. 1

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Outcome measures

Assessments were performed using clinical tools [box and block test (BBT), Jebsen–Taylor hand function test (JTHFT), and HGS] to evaluate the hand dexterity and function in daily life, and kinematic data were collected from a three-dimensional analysis system during the forward-reaching task. All measurements were performed in the affected upper limb.

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The box and block test

The BBT aims to examine the dexterity of the hands. Scores indicate the number of wooden cubes (2.54 cm/side) carried from one box to the other in 1 min (Trombly and Radomski, 2002). To perform the BBT, patients were instructed to carry the cubes using the thumb and the index finger as many times as possible. Previous studies have reported the BBT to be reliable for use in clinical settings (Platz et al., 2005).

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The Jebsen–Taylor hand function test

The JTHFT is a simple, objective test of hand function used frequently in daily routine activities, which includes seven items (turning over cards, picking up small objects, stacking checkers, picking up beans with a spoon, turning over large empty cans, turning over large weighted cans, and handwriting). Each item is performed separately and timed, and the score is calculated as the total time of all seven items. The JTHFT has been shown to be reliable (Jebsen et al., 1969).

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Hand grip strength

A JAMAR hydraulic dynamometer (Sammons Preston Rolyan, Chicago, Illinois, USA) was used to measure HGS. For the measurement, patients were asked to hold the handle of the dynamometer with the affected hand, standing with feet shoulder width apart, and then squeeze as hard as possible (Roberts et al., 2011). Measurement data were averaged over three repetitions with a 1-min interval between each repetition (Chen et al., 2009).

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Kinematic data recording

An ultrasound movement analysis system (CMS 10 Measuring System; Zebris Medical GmbH, Isny, Germany) was used to measure quantitative data [peak velocity and movement distance at sagittal (X), coronal (Y), and horizontal (Z) planes] of wrist movement during forward reaching. The system consisted of ultrasound emitting markers (1 cm in diameter placed on the middle portion of the wrist joint) (Blank et al., 2008), a detector and cable adapter to recognize and convey ultrasound signals from the markers, and a recording panel containing three microphones to measure the marker movement in three-dimensional space. The sampling rate for collecting spatial data was a frequency of 15 Hz with a spatial resolution of 0.01 mm. The starting position for the measurement was sitting in a comfortable chair (individually adjustable for height and distance) with the wrist neutral, elbows flexed 90°, and upper arms at the side. Patients sat on the chair against the backrest, and the experimental table was positioned in front of the chair to guide the forward-reaching task. Patients’ trunk was strapped to the backrest of the chair to avoid compensatory motion during the reaching task (Blank et al., 2008). Two 10-cm lines, 25 cm apart, were drawn on the table to mark the starting and target points for performing the forward-reaching task. Patients were instructed to reach their affected hand toward the target point without touching the table. Data were averaged over five trials with a 1-min interval between each trial.

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Experimental procedures

The somatosensory stimulation procedure included four experimental options: (a) no stimulation, (b) vibration, (c) light touch, and (d) rough touch. These options were crossed randomly over for their application, with just one option per day for 4 days to avoid a carryover effect of the somatosensory stimulations. Randomization for the application of somatosensory stimulation was determined by blindly drawing one card from an envelope with four cards marked 1, 2, 3, and 4. Patients were asked to sit in a chair with their elbow flexed 90° and forearm supinated. All the sensory stimulation procedures were performed on the volar surface of the hand and forearm of the affected side for 5 min (30 trials of sensory stimulation at a moving speed averaging 0.05 m/s) by applying the stimulation from the finger tips, palm, and wrist to forearm (distal to proximal) to stimulate underlying superficial and deep sensory receptors, as suggested by the somatosensory testing procedure (Conrad et al., 2011). Vibration was applied at a frequency of 80 Hz using a vibration device (Thrive MD-01; Thrive Co. Ltd, Osaka, Japan). The application of light and rough touches followed the method (Brasil-Neto and de Lima, 2008) using a brush (medium; Therapressure, San Francisco, California, USA) and sandpaper (medium-grain; Daesung, Seoul, Korea), respectively. Light and rough touch stimulations were provided with a 30° inclination of the ends of the brush and sandpaper to the skin surface. When patients complained of any discomfort during somatosensory stimulation, the stimulation was discontinued. Measurements were performed before and after the 5-min somatosensory stimulation, and changes between pretest and post-test were used for data analysis.

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Data analysis

Statistical analysis was carried out using the SPSS 12.0 software (SPSS Inc., Chicago, Illinois, USA). The changes in pretest and post-test data were represented as the median and interquartile range. The effects of the four experimental conditions were compared using the Friedman test, and when a statistical significance was found, Tukey’s post-hoc test was used for multiple pairwise comparisons. The level of significance was set at 0.05.

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Results

Changes in hand function after somatosensory stimulation

Table 1 shows the findings of the BBT, JTHFT, and HGS. There were significantly different BBT and JTHFT scores and HGS between the types of somatosensory stimulation (P<0.05). In the post-hoc test, the BBT and JTHFT scores appeared to be higher for vibration, light touch, and rough touch than those for no stimulation. The JTHFT score was significantly greater for vibration than that for rough touch. In addition, the HGS appeared to be significantly greater for light touch than that for no stimulation and for vibration than that for light touch.

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Changes in peak velocity and movement distance at the wrist after somatosensory stimulation

Table 2 summarizes the outcomes of the movement distance and peak velocity at the wrist between the types of somatosensory stimulation. Significant differences were found for the sagittal and coronal planes in the movement distance and for the sagittal and horizontal planes in the peak velocity (P<0.05). In the post-hoc test, the movement distance in the sagittal plane was significantly greater for vibration, light touch, and rough touch than that for no stimulation. The movement distance in the coronal plane was significantly greater for vibration than that for light and rough touches and for no stimulation. Compared with the movement distance in the coronal plane for no stimulation, those for light and rough touches appeared to be significantly greater. The peak velocity in the sagittal plane was significantly greater for rough touch and vibration than that for no stimulation, for vibration and rough touch than that for light touch. The peak velocity in the horizontal plane was significantly greater for vibration and light and rough touches than that for no stimulation, and for vibration than that for light and rough touches (Table 3).

Table 2

Table 2

Table 3

Table 3

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Discussion

The findings of the current study suggest that the use of somatosensory stimulation on the hand and forearm may be helpful for enhancing hand function and movement, with more favorable effects observed using muscle vibration than light and rough touches.

In general, tactile input has been shown to be a beneficial option to guide hand function of patients with poststroke hemiparesis (Kwon and Jang, 2011). On the basis of previous research, the present study adopted several types of tactile stimulation (a soft brush, sandpaper, and vibration) applied on the volar side of the forearm in a distal-to-proximal direction. These types of stimulation provide an opportunity to avoid misperceiving them as noxious stimuli and to adequately discriminate the properties of tactile stimuli. Furthermore, our choice of vibration application included the optimum range of its frequency to induce a muscular response (van den Berg et al., 2010). The main focus of the current study was to explore the clinical benefits of somatosensory stimulation in patients with poststroke hemiparesis. To achieve this goal, we used clinical tools to measure upper limb function, which have been used frequently in a clinical setting. However, given that these tools report the functional outcome by scoring performance on the basis of observation, it may be difficult to obtain specific knowledge related to movement pattern and performance strategy from their uses in study procedure (Alt Murphy et al., 2011). In the present study, involvement of kinematic data (movement distance and peak velocity) during the forward-reaching task that is commonly required in everyday activities is valuable to support the outcome obtained from the clinical assessment tools because it identifies the movement pattern in space and provides better knowledge of movement changes (Alt Murphy et al., 2011).

In the current study, the findings support the use of somatosensory stimulation such as light and rough touches and vibration. Somatosensory stimulation has been commonly proposed as a possible therapeutic option to improve the ability to perform hand tasks, thereby enhancing the training effects on motor function after stroke (Ikuno et al., 2012). Cutaneous input induced from the hand and finger facilitates the reflex processing mechanism in segmental spinal pathways involving intersegmental neurons, which regulate movement control of the upper limb and modulate grip force (Yousef et al., 2011). After a stroke, motor recovery relies on the reorganization of motor (Wang et al., 2010) and somatosensory cortices (Roiha et al., 2011). As somatosensory afferent input has been known to modulate the cortical excitability of the motor area (Laaksonen et al., 2012), the integration of well-organized somatosensory input with motor programs may be considered an important contributing factor to regain normal motor function.

As shown in the current study, the results imply that vibration stimulation may be more favorably used to enhance the clinical function of the affected upper limb in patients with poststroke hemiparesis with improved spatiotemporal acuity during the forward-reaching task. A possible explanation for the observed gains with vibration stimulation may be that the facilitation of the firing of muscle spindle’s Ia afferents results in enhancement of corticospinal excitability and causes increased activity of the Ia inhibitory interneurons. As a result, the reflex threshold of the paretic limb is progressively reduced (Libouton et al., 2012), thereby leading to optimization of the control mechanism of muscular coactivation during actual limb movements (Trumbower et al., 2010). The present study supports the results of a previous study suggesting the beneficial long-term effects of a focal muscle vibration, which is applied repeatedly at a frequency of 100 Hz for 90 min over 3 consecutive days, on motor performance in patients with poststroke hemiparesis (Caliandro et al., 2012). In addition, the current results are similar to those of recent studies that reported positive changes in motor control during functional tasks (Liepert and Binder, 2010).

Muscle vibration provides additional opportunity for strong proprioceptive stimulation by reaching the sensorimotor cortex directly (Christova et al., 2011) and facilitating cortical reorganization, which can improve cortical influence on motor systems (Zhao et al., 2011). Recruitment of cortical neurons is probably because of the integration of somatosensory inputs, which facilitates the planning process of limb movements and regulates the potential involvement of adjacent joints. Moreover, another assumption of vibration effects is caused by repetitive tactile stimulation on skin, which results in benefits from synchronous activation in neural afferents and cortical neurons and influences the connectivity of cortical neurons in the sensory cortex with the neural network of other cortices (Freyer et al., 2012). After vibration stimulation, increased cortical excitability has been evidenced by numerous neuroscientific studies (Conrad et al., 2011). Such a neurophysiological correlation may be the possible mechanism for long-term potentiation derived from alterations in the strength of the corticocortical connections (Hoogendam et al., 2010). Enhanced cortical activity of the motor area may be a contributing factor to enhance the fidelity of movement control during the initial phase of rehabilitation such as the feedforward mechanism and anticipatory motor control. Subsequently, spinal reflex systems may be effectively modulated by facilitation in descending cortical control (Conrad et al., 2011). The reinforcement of cortical activation contributes toward the increase in motor-evoked potential and decrease in latency of the vibrated muscle, which is observed early after the onset of the vibration (Christova et al., 2011). These results suggest that our findings may be useful for research that investigates the effects of vibration on the recovery of somatosensory deficits and improvement of function after treatment, although a single application of sensory stimulation cannot affect brain plasticity.

In addition, a changed muscular response derived from the vibration stimulation can alter the spastic property of upper limb muscles (Zhao et al., 2011). Knowledge of these mechanisms may be useful for performing vibration stimulation as a daily routine therapy of stroke rehabilitation. In general, fine motor control and hand dexterity are the primary means of successfully executing skillful, voluntary movements, which is based on the ability to accept, precisely perceive, and discriminate sensory stimuli received from external environmental sources. Improved hand function may be the main factor allowing the ability to independently perform everyday tasks, leading to a huge impact on the quality of life (Carey et al., 1993). Therefore, the implication is that the use of sensory training contributes toward the transfer of its effects to daily, routine activities and functional recovery.

Despite the favorable effects of somatosensory stimulation, the current study has some limitations that can be improved upon by further studies. First, the small sample size may be a major limiting factor in establishing the generality of the results to the entire population of patients with poststroke hemiparesis. Second, the current study suggests that there are immediate effects of a single dose of sensory stimulation and the potential for further effects with treatment; therefore, we acknowledge that the findings of the study cannot be described as the long-term effects of somatosensory stimulation owing to the lack of follow-up data, and it may be difficult to understand the findings beyond our procedures of somatosensory stimulation. Third, this study did not include an assessment tool to examine the perceived level of tactile sensation for the patient’s selection; therefore, the findings were not free from its influences. Finally, although each type of somatosensory stimulation was applied with a 1-day interval to avoid a carryover effect, it may be difficult to ensure the independence of their effects completely. Robust studies with a larger sample size and a longer follow-up period should be carried out to support the findings of the current study in this field.

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Conclusion

Somatosensory stimulation is commonly known to be useful for overcoming the learned nonuse of the affected upper limb and thereby improving the performance level in everyday activities. Our findings confirm that the use of somatosensory stimulation on the hand and forearm may be beneficial to improve hand function and movement in patients with poststroke hemiparesis, with more favorable effects observed using muscle vibration than light and rough touches. It provides useful information for clinicians and researchers who explore extra therapeutic options for improving hand function in stroke rehabilitation.

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Acknowledgements

Conflicts of interest

There are no conflicts of interest.

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Keywords:

hand function; somatosensory stimulation; stroke

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