PM R xx (2014) 1-9
www.pmrjournal.org
Original Research
Do Textured Insoles Affect Postural Control and Spatiotemporal Parameters of Gait and Plantar Sensation in People With Multiple Sclerosis? Alon Kalron, PhD, Diana Pasitselsky, BPT, Michal Greenberg-Abrahami, MA, Anat Achiron, MD, PhD
Abstract Background: Balance and gait deficits are common in people with multiple sclerosis (MS). Physical interventions directed at improving balance and walking abilities have been implemented using various approaches. Nonetheless, no mode of training has been universally agreed upon. Objectives: To determine whether textured insoles have immediate effects on postural control and spatiotemporal parameters of gait and plantar sensation in people with people with MS and to explore effects 4 weeks after insole wear as to whether any immediate effects are maintained over time. Design: Within-subject experimental study with a 4-week intervention phase. Settings: Multiple Sclerosis Center, Center of Advanced Technologies in Rehabilitation, Sheba Medical Center, Tel-Hashomer, Israel. Participants: Twenty-five relapsing-remitting patients diagnosed with MS, 16 women and 9 men, aged 49.6 years (standard deviation ¼ 6.5 years). Intervention: Textured insoles customized according to foot size and adapted to the participant’s casual shoes. Main outcome measures: Spatiotemporal parameters of gait and center of pressure (CoP) excursions during static postural control were studied using the Zebris FDM-T Treadmill. Light-touch and pressure-sensation thresholds were determined using the Semmes-Weinstein monofilaments test. Results: Textured insoles did not alter static postural control parameters when examined with eyes open. Examination during the eyes-closed task demonstrated an immediate reduction in the CoP path length (298.4 mm, standard error ¼ 49.7 mm, versus 369.9 mm, SE ¼ 56.3 mm; P ¼.04) and sway rate (12.0 mm/s, standard error ¼ 1.4 mm/s, versus 15.1 mm/s, standard error ¼ 1.6 mm/s; P ¼ .03) after insertion of the textured insoles compared to casual shoes alone. These findings were maintained at termination of the insole 4-week intervention period. In terms of spatiotemporal parameters of gait, differences were not observed between casual shoes and shoes with textured insoles at baseline. Likewise, no differences were observed between initial and concluding gait trials. Significant differences in plantar sensitivity measures were not observed after the insole 4-week intervention phase. Conclusions: Although there were improvements in some aspects of balance, the efficacy of textured insoles in the MS population remains unclear.
Introduction Balance and gait deficits are common in people with multiple sclerosis (MS). These very disabling deficits reduce mobility and independence, lead to falls and injuries, and negatively affect quality of life [1-3]. In general, physical interventions directed at improving balance and walking abilities have implemented various approaches: for example, motor and sensory strategies [4], Feldenkrais exercises [5],
robot-assisted gait training [6], kickboxing [7], Pilates exercises [8], Ai-Chi exercises [9], Nintendo Wii games [10], strength and aerobic training [11], and neuromuscular facilitation [12,13]. Nevertheless, no mode of training has been universally agreed upon. Moreover, although PwMS use many fall prevention tactics, they nonetheless frequently fall [14]. Thus, additional types of intervention strategies aimed at improving balance and walking for people with MS should be considered.
1934-1482/$ - see front matter ª 2014 by the American Academy of Physical Medicine and Rehabilitation http://dx.doi.org/10.1016/j.pmrj.2014.08.942
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Textured Insoles in MS
It has been shown that feedback from plantar cutaneous afferents is important for the maintenance of normal balance when vision is inaccessible [15]. In addition, foot sole input contributes to the coding and the spatial representation of body posture [16]. Therefore, theoretically, wearing textured insoles can affect gait and balance by increased stimulation to the plantar surface of the feet, thereby influencing neuromuscular function. Several studies have reported that textured insoles reduce postural sway during standing in healthy young [17] and older [18-20] people. However, other studies have shown no clear benefit to healthy people [21] and older individuals who fall [22], during similar gait and balance tasks. It is well known that somatosensory deficit is a common feature of MS. Furthermore, previous trials have demonstrated that slowed spinal somatosensory conduction in people with MS while standing leads to extremely delayed postural responses [23]. Therefore, it is reasonable to consider textured insoles as an intervention alternative aimed at improving gait and balance abilities in people with MS. To date, there has been limited research as to the effects of textured insoles on mobility performance in the MS population [24,25]. According to our literature investigation, 2 studies examined this intervention strategy in PwMS. Kelleher et al, in a small study of 14 patients with MS, reported several effects on gait kinematics and kinetics, including benefits to knee and hip excursion, and ground reaction forces when wearing textured insoles constructed from sandpaper [24]. Conversely, no immediate effects were demonstrated in gait and balance performance in a group of 46 patients with MS who wore textured insoles. However, following a 2-week intervention phase of insole wear, improvements were observed in spatiotemporal parameters of gait [25], although it was unclear whether the response was a placebo or learning effect. It remains unclear as to whether textured insoles modify gait and balance performance and plantar sensation immediately and in the long term in people with MS. Given this knowledge, the purpose of the current study was 2-fold: (1) to determine whether textured insoles have immediate effects on postural control, spatiotemporal parameters of gait, and plantar sensation in people with MS; and (2) to explore effects 4 weeks after wearing the insoles as to whether any immediate effects are maintained over time.
were recruited from the Multiple Sclerosis Center, Sheba Medical Center, Tel-Hashomer, Israel. Inclusion criteria included a neurologist-confirmed diagnosis of definite relapsing-remitting MS according to the revised McDonald criteria [26]; the ability to walk without an assistive device (eg, a cane or walker); and relapse-free for at least 30 days before testing. Exclusion criteria included orthopedic disorders that could negatively affect mobility; major depression or cognitive decline; pregnancy; blurred vision; cardiovascular disorders; peripheral neuropathy; and diabetes. All patients were characterized by mobility difficulties confirmed by a neurological examination. Patients were then scored according to the Expanded Disability Status Scale (EDSS), an accepted method of quantifying disability in MS [24]. Ethical approval for the study was obtained by the Sheba Institutional Review Board. All participants signed an informed consent form. Textured Insoles Insoles were customized for both left and right feet according to the participant’s foot width and length. The insoles were 3 mm thick and made of elastic rubber and fabric. The coarse texture of the insole was designed with miniature square pyramids organized in a grid pattern (Figure 1). This material and design proved favorable, as it was considered sufficiently rough to provide sensory feedback, yet not rough enough to cause skin discomfort. Sensory Evaluation Light-touch and pressure-sensation thresholds were determined using the Semmes-Weinstein monofilaments test [27]. This measurement is a standardized test commonly used in research and sensory evaluation of peripheral and central nerve lesions and is usually used
Methods Study Participants This was a within-subject experimental study with a 4-week intervention phase. Twenty-five relapsingremitting patients diagnosed with MS, 16 women and 9 men, aged 49.6 years (standard deviation ¼ 6.5 years)
Figure 1. Insole designed with miniature square pyramids organized in a grid pattern.
A. Kalron et al. / PM R xx (2014) 1-9
as a criterion standard of touch-pressure threshold and tactile sensation. The sensory test was performed on 3 locations on the plantar surface of each foot: heel, medial forefoot, and lateral forefoot. A modified 4, 2, and 1 stepping algorithm [28] was used to evaluate the threshold point. The subjects lay prone, unable to observe the test procedure. The monofilaments test began with a size 4.17 filament. Depending on the subject’s response, the changes in stimulus intensity were executed in 3 increments until a change in their response was observed and a turnaround point reached. Changes were then made in 2 increments until another turnaround point, at which point all stimuli was presented into 1 increment. The tactile sensation threshold was determined as the lightest filament experienced >50% of the time. For each location tested, the examiner performed 2 null trials randomly placed throughout the algorithm. If the subject responded to both null trials at any given location, the test was halted and the subject reinstructed. Gait Analysis Spatiotemporal parameters of gait were studied using the Zebris FDM-T Treadmill (Zebris Medical GmbH, Germany). The Zebris FDM-T is fitted with an electronic mat of 10 240 miniature force sensors, each approximately 0.85 0.85 cm, embedded underneath the belt. The treadmill’s contact surface measures 150 50 cm, and its speed can be adjusted from 0.2 and 22 km/h, at intervals of 0.1 km/h. When the subject stands or walks on the treadmill, the force exerted by the feet (the socalled reactive-normal force in directions x, y, and z) is recorded by the sensors at a sampling rate of 120 Hz. Due to the high density of the sensors, the foot is mapped at a high resolution to facilitate even subtle changes in force distribution. Timing can also be monitored. Dedicated software integrates the force signals and provides 2-dimensional/3-dimensional graphic representation of major spatiotemporal parameters including center of pressure (CoP) trajectories during gait. In addition, we collected and analyzed the coefficient of variation (CV ¼ SD/mean) scores of step length and step time. The CV (%) is an acceptable relative measure of the intraindividual variability of spatiotemporal parameters of gait. The magnitude of the CV percentage corresponds to greater variability of the selected spatio-temporal parameter. Walking on an instrumented treadmill has several advantages compared to an over-ground device with similar footprint analysis capability. Specifically, compared to the electronic walkway, treadmill gait analysis is not limited to the number of steps per trial, thus enabling gait analysis over large distances. We assume that this ability is essential in the MS population because of fatigue concerns.
3
In 2012, Faude et al reported high levels of betweenand within-day reliability in healthy seniors for the majority of spatiotemporal gait parameters recorded by the Zebris Treadmill system during walking, with coefficients of variation typically less t han 5% and 7%, respectively [29]. Recently, the instrumented treadmill has been found to be an appropriate tool for assessing ambulation capabilities in people with MS. Furthermore, spatiotemporal gait parameters collected by this device during walking seem to be valid markers of neurological impairment in the MS population [30]. Static Postural Control Assessment Similar to gait analysis, static postural control parameters were obtained using the Zebris FDM-T Treadmill. A set of outcome measures taken from the CoP data during static stance were as follows: (1) ellipse sway area (mm2), defined as the 95% confidence ellipse for the mean of the CoP anterior, posterior, medial, and lateral coordinates; (2) CoP path length (mm), defined as the absolute length of the CoP path movements over the testing period; (3) sway rate (mm/s), defined as the mean speed of movement of the CoP during the testing period; and (4) average pressure distribution of the left and right foot expressed in bodyweight (%). Accordingly, the bilateral pressure distribution asymmetry score was calculated as the absolute difference in pressure distribution between legs. In a perfect symmetrical stance, this variable is 0. Experimental Design Upon acceptance into the study, each participant received a pair of textured insoles customized according to foot size and adapted to the participant’s casual shoes. The textured insoles were placed with the rigid texture in direct contact with the patient’s sole. Subsequently, the subjects completed a set of baseline measurements. Tests included sensory evaluation of both feet, followed by an examination of static postural control and gait. The last 2 examinations were carried out twice, wearing either casual shoes or casual shoes with the textured insoles. Before the treadmill gait measurement phase, all participants actively participated in an adaptationfamiliarization trial to establish the speed level of each individual. Starting at a fixed speed of 0.5 km/h, belt speed was increased by 0.3 km/h every 15 seconds, in a stepwise manner. When the participant informed the tester which speed best characterized that participant’s normal walking pace, that speed was designated as that individual’s comfort speed. After this adaptation phase, each participant was instructed to walk on the treadmill for 1 consecutive minute at the participant’s comfort speed. According to the participant’s
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Textured Insoles in MS
stride lengths, the amount of gait cycles included in the analysis ranged between 45 and 60. Posturography was carried out in the following manner. Each subject completed a sequence of 3 consecutive postural control tests under 3 different task conditions with a 1-minute break between tasks. Each task was repeated 3 times, for 20 seconds, followed by a 30-second rest period, as follows: (1) Eyes open: Subjects stood on the treadmill belt (10-cm gap between heels; 5 toe-out position), in an upright static position with arms resting at their sides. Participants were instructed to maintain their posture as steady as possible while visually focusing on a dot marked 1 m located directly in front of them. (2) Eyes closed: Conditions were identical to those of the eyes-open task but with eyes closed. (3) Narrowed base: Conditions were identical to those of the eyes-open task but with legs together. All measurements were performed at the Center of Advanced Technologies in Rehabilitation, Sheba Medical Center. Measurements were completed by an experienced physical therapist specialized in neurological rehabilitation. At termination of baseline measurements, textured insoles were provided. Participants were instructed to wear the textured insoles constantly throughout the day and to continue with their regular activities for 4 consecutive weeks. A physical therapist telephoned each person at the end of the first, second, and third week to detect possible difficulties or complaints encountered with the textured insoles. Re-assessment of standing balance, gait, and plantar sensation was completed after 4 weeks using the same procedures used at the first assessment. Statistical Analysis Descriptive statistics were performed to determine distributions of demographic, clinical, sensory, postural control, and gait parameters. All sensory and motor performance data were normally distributed according to the Kolmogorov-Smirnov test. The Spearman rho correlation analysis assessed the relationship between major postural control parameters to sensory evaluation measurements collected at baseline. Paired-samples t tests were performed to determine whether textured insoles had any immediate effects on postural control and spatiotemporal parameters of gait, and whether the 4-week intervention phase had any effects on postural control, spatiotemporal parameters of gait, and plantar sensation. Comparison between baseline and termination of the intervention program was based on measurements taken while wearing casual shoes without insoles. All analyses were performed using IBM SPSS statistics software (version 21.0 for Windows; IBM, Armonk, NY). All reported P values were 2 tailed. The level of significance was set at P < .05.
Table 1 Descriptive characteristics of study participants (n ¼ 25) Variable
Mean (SD)
Age, y Gender Male Female Ratio male/female Disease duration, y EDSS Pyramidal Cerebellar Visual Brainstem Cerebral Sensory
49.6 (6.5) 9 16 0.56 10.2 (7.5) 3.4 (3.0) 1.8 (1.0) 1.1 (1.0) 0.3 (0.5) 0.2 (0.5) 0.3 (0.5) 0.9 (1.0)
SD ¼ standard deviation; EDSS ¼ Expanded Disability Status Scale.
Results Descriptive characteristics of study participants are provided in Table 1. Significant Spearman rho correlation scores were shown between sensory evaluation measurements to the CoP path length and sway rate in the diverse condition tasks (eyes open, eyes closed, and legs together) (Table 2). These findings reinforce the main assumption of the present study that reduced plantar sensation is connected with poor balance control. The participants did not report any new neurological exacerbations during the experimental period. According to information obtained via telephone follow-up, no one asked to withdraw from the study. All participants reported that they had followed the study instructions regarding wearing of the textured insoles throughout the 4-week experimental period. Three patients reported mild disturbance related to insole wearing during the first week of the trial, but this resolved during the second week. Textured insoles did not alter static postural control parameters when examined with eyes open and at a narrowed base position. Static postural control parameters were also not altered at the immediate response phase and after the 4-week intervention. Nevertheless, examination during the eyes closed task demonstrated an immediate reduction in the CoP path length (298.4 mm, SE ¼ 49.7 mm, versus 369.9 mm, SE ¼ 56.3 mm; P ¼ .04) and sway rate (12.0 mm/s, SE ¼ 1.4 mm/s versus 15.1 mm/s, SE ¼ 1.6 mm/s, P ¼ .03) after insertion of textured insoles compared to wearing casual shoes without insoles. Moreover, these findings were maintained at termination of the insole 4-week intervention period. Static postural control performance at baseline is presented in Table 3. Postural control statistics after the 4-week insole intervention effects are presented in Table 4. In terms of mean and variability spatiotemporal parameters of gait, differences were not observed at
A. Kalron et al. / PM R xx (2014) 1-9
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Table 2 Spearman rho correlation scores (P values) between sensory evaluation and major postural control parameters at baseline Task Condition
Open
Plantar Sensation Area
CoP
Sway Rate
CoP
Sway Rate
CoP
Sway Rate
.433 (.004) .513 (.001) .497 (.001)
.428 (.004) .516 (.001) .491 (.001)
.361 (.017) .311 (.043) .380 (.012)
.355 (.020) .308 (.045) .373 (.014)
.371 (.014) .421 (.027) .410 (.010)
.395 (.023) .368 (.005) .393 (.019)
.353 (.042) .574 (.001) .453 (.001)
.348 (.007) .573 (.001) .421 (.014)
.361 (.017) .430 (.004) .391 (.017)
.355 (.020) .426 (.004) .385 (.042)
.376 (.017) .330 (.034) .378 (.017)
.295 (.040) .429 (.035) .375 (.020)
Right Heel Medial forefoot Lateral forefoot Left Heel Medial forefoot Lateral forefoot
Closed
Legs Together
CoP ¼ center of pressure.
baseline between casual shoes and shoes with textured insoles. Likewise, no differences were observed between initial and concluding gait trials. Spatiotemporal gait outcomes in relationship to immediate wear of insoles (Table 5) and following the 4-week intervention period (Table 6) are presented. Significant differences in plantar sensitivity measures were not observed following the insole 4-week intervention phase. Sensory outcomes, defined by the Semmes-Weinstein monofilaments test at baseline and at termination of the intervention period were as follows: right heel (4.3, SE ¼ 0.2, versus 4.1 SE ¼ 0.3; P ¼ .60); right lateral forefoot (4.0, SE ¼ 0.2 versus 3.8, SE ¼ 0.2; P ¼ .38); right medial forefoot (4.0, SE ¼ 0.2, versus 4.1, SE ¼ 0.3); P ¼ .43); left heel (4.4, SE ¼ 0.2, versus 3.9, SE ¼ 0.2; P ¼ .34); left lateral forefoot (4.1, SE ¼ 0.3, versus 3.9, SE ¼ 0.2; P ¼ .51); and left medial forefoot (4.2, SE ¼ 0.2, versus 4.0, SE ¼ 0.2; P ¼ .61). Discussion The primary aim of the current study was to determine whether textured insoles affect postural control and gait in people with MS. Mobility parameters
were examined at 2 time points: immediately after wearing the insoles, and after a 4-week intervention period. Furthermore, we examined whether the 4-week intervention program altered plantar sensation. The underlying principle of the use of textured surfaces was to enhance sensory input. There is much debate relating to the effect of footwear on gait and postural control in various populations. According to our results, the efficacy of textured insoles remains unclear. Moreover, it is unclear whether textured insoles should be recommended for people with MS who have mobility impairments. On one hand, textured insoles had no effect on spatiotemporal parameters of gait, immediately and after the intervention period. Similar findings were observed with plantar sensation. Conversely, we found a reduction in several postural control variables, including CoP path length and sway rate performed with closed eyes, immediately and at termination of the insole intervention program. Importantly, these parameters have been found to correlate with balance performance and risk of falls in people with MS [3,31]. Recently, Prosperini et al found that, in people with MS, CoP trajectories measured during static stance were correlated with worse diffusion-tensor imaging parameters along the cerebellar
Table 3 Static postural control performance with shoes compared to shoes with insoles at baseline Mean (SE) Task Condition Eyes open
Eyes closed
Narrowed base
Postural Variable
Shoes 2
Ellipse sway area, mm CoP path length, mm Sway rate, mm/s Pressure distribution difference (%) Ellipse sway area, mm2 CoP path length, mm Sway rate, mm/s Pressure distribution difference, % Ellipse sway area, mm2 CoP path length, mm Sway rate, mm/s
SE ¼ standard error; CoP ¼ center of pressure. * P < .05.
165.4 256.1 12.9 9.6 267.1 369.9 15.1 12.0 198.9 309.9 15.5
(53.7) (45.4) (2.3) (1.4) (59.3) (56.3) (1.6) (1.8) (34.4) (31.5) (1.7)
Insoles
Mean Difference (SE)
P value
185.4 276.4 13.9 11.8 199.8 298.4 12.0 12.4 224.6 321.1 16.6
20.0 20.3 0.9 2.1 67.3 71.5 3.8 0.4 25.6 11.2 1.1
.50 .24 .29 .17 .12 .04* .03* .83 .25 .45 .24
(38.2) (35.2) (1.9) (2.0) (44.4) (49.7) (1.4) (2.5) (37.8) (35.1) (1.7)
(25.9) (16.8) (0.8) (1.5) (41.2) (32.3) (1.6) (1.6) (21.8) (14.7) (0.8)
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Textured Insoles in MS
Table 4 Static postural control performance at baseline and after the 4-week intervention period Mean (SE) Task Condition Eyes open
Eyes closed
Narrowed base
Postural Variable 2
Ellipse sway area (mm ) CoP path length (mm) Sway rate (mm/s) Pressure distribution difference (%) Ellipse sway area (mm2) CoP path length (mm) Sway rate (mm/s) Pressure distribution difference (%) Ellipse sway area (mm2) CoP path length (mm) Sway rate (mm/s)
Baseline
Post-intervention
Mean Difference (SE)
P value
165.4 256.1 12.9 9.6 267.1 369.9 15.1 12.0 198.9 309.9 15.5
148.8 242.0 12.3 11.4 162.7 302.1 12.3 11.2 181.6 312.5 15.9
16.8 14.1 0.6 1.8 104.4 67.8 2.8 0.8 17.3 2.6 0.4
.33 .25 .29 .46 .04* .03* .03* .39 .43 .78 .62
(53.7) (45.4) (2.3) (1.4) (59.3) (56.3) (1.6) (1.8) (34.4) (31.5) (1.7)
(38.3) (39.5) (2.0) (2.7) (32.9) (42.3) (1.2) (2.1) (29.6) (30.7) (1.6)
(22.3) (12.7) (0.7) (1.9) (31.6) (28.7) (1.1) (1.0) (22.7) (15.1) (1.4)
SE ¼ standard error; CoP ¼ center of pressure. * P < .05.
connections and supratentorial associative white matter bundles. Gray matter atrophy of the superior lobules of the cerebellum (IV, V, VI) and lobules VIII also correlated with worse posturometric values [32]. Nevertheless, no changes in postural control were observed when examined with eyes open. To the best of the authors’ knowledge, no more than 2 studies have explored the efficacy of footwear intervention on gait and balance in the MS population [24,25]. Although there are differences between our and previous studies, mainly in terms of study design and outcome measures, we found the comparison worth discussing. Dixon et al [25] reported that textured insoles had no significant immediate effect on gait variables compared with control conditions. However, they reported that after the 2-week intervention period, the insole intervention group demonstrated an increase in step and stride length. In contrast, the
current study data did not attest to significant changes in 14 (of 14) spatiotemporal parameters of gait after the 4-week intervention phase. We assume that the different measurement devices between our study and that of Dixon et al may have been the cause of this dissimilarity. Whereas Dixon et al [25] measured over-ground gait using an electronic walkway, we collected spatiotemporal parameters of gait with an instrumented treadmill. The main difference between measurement procedures relates to control of the participants’ walking speed. The instrumented treadmill enables the examiner to control velocity of gait. Accordingly, in the present study, speed of walking was defined at baseline and was preset for all other gait trials, including at the completion of the intervention program. In contrast, control of speed with over-ground measurement equipment is not possible; that is, speed of
Table 5 Spatiotemporal gait outcomes with shoes compared to shoes with insoles at baseline Mean (SE) Gait Variable
Shoes
Insoles
Mean Difference (SE)
P value
Velocity, km/h Cadence, steps/min Step time R, s Step time L, s CV step time R, % CV step time L, % Step length R, cm Step length L, cm CV step time R, % CV step time L, % Stance R, % GC Stance L, % GC Single support R, % GC Single support L, % GC Double support, % GC Stride time, s Stride length, cm Step width, cm
2.5 96.7 0.63 0.63 3.6 3.4 42.9 42.8 3.5 3.8 69.0 68.9 31.1 31.0 37.9 1.26 85.7 11.7
2.5 95.7 0.65 0.66 3.7 3.2 41.4 41.5 3.4 3.7 69.3 68.7 31.3 30.7 38.0 1.30 82.9 11.3
0.005 1.0 0.02 0.03 0.1 0.2 1.5 1.3 0.1 0.1 0.3 0.2 0.2 0.3 0.1 0.04 2.8 0.4
.45 .19 .38 .27 .86 .74 .43 .21 .56 .78 .12 .12 .18 .21 .22 .07 .09 .24
(0.2) (2.7) (0.02) (0.02) (2.1) (2.8) (3.2) (3.1) (2.3) (2.2) (0.8) (1.0) (1.0) (0.8) (1.7) (0.03) (6.2) (0.7)
(0.2) (3.3) (0.03) (0.03) (2.4) (1.9) (2.7) (2.7) (2.7) (2.1) (0.7) (0.8) (1.6) (0.7) (1.5) (0.05) (5.4) (0.7)
SE ¼ standard error; R ¼ Right; L ¼ Left; CV ¼ coefficient of variation; GC ¼ gait cycle.
(0.1) (0.9) (0.09) (0.09) (1.3) (1.5) (2.0) (1.1) (1.4) (1.3) (0.6) (0.6) (0.8) (0.8) (1.0) (0.02) (4.1) (0.3)
A. Kalron et al. / PM R xx (2014) 1-9
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Table 6 Spatiotemporal gait outcomes at baseline and after the 4-week intervention period Mean (SE) Gait Variable
Baseline
Post-intervention
Mean Difference (SE)
P value
Velocity, km/h Cadence, steps/min Step time R, sec Step time L, sec CV step time R, % CV step time L, % Step length R, cm Step length L, cm CV step time R, % CV step time L, % Stance R, % GC Stance L, % GC Single support R, % GC Single support L, % GC Double support, % GC Stride time, s Stride length, cm Step width, cm
2.5 96.7 0.63 0.63 3.6 3.4 42.9 42.8 3.5 3.8 69.0 68.9 31.1 31.0 37.9 1.26 85.7 11.7
2.5 100.2 0.61 0.62 3.3 3.2 41.5 41.2 3.6 3.7 69.3 68.6 31.4 30.7 37.9 1.23 82.8 11.3
0.005 3.5 0.02 0.001 0.3 0.2 1.4 1.5 0.1 0.1 0.3 0.3 0.3 0.3 0.03 0.03 2.9 0.4
.98 .21 .26 .66 .45 .59 .60 .58 .88 .69 .66 .62 .60 .71 .98 .44 .59 .27
(0.2) (2.7) (0.02) (0.02) (2.1) (2.8) (3.2) (3.1) (2.3) (2.2) (0.8) (1.0) (1.0) (0.8) (1.7) (0.03) (6.2) (0.7)
(0.3) (3.3) (0.02) (0.03) (2.3) (2.7) (3.4) (3.6) (2.9) (2.2) (1.0) (1.0) (1.0) (1.0) (2.0) (0.05) (7.0) (0.7)
(0.16) (2.7) (0.02) (0.09) (1.9) (1.8) (2.5) (2.7) (2.1) (1.8) (0.7) (0.6) (0.6) (0.7) (1.3) (0.04) (5.2) (0.4)
SE ¼ standard error; R ¼ right; L ¼ left; CV ¼ coefficient of variation; GC ¼ gait cycle.
walking is independent for each gait test. The differences in the speed control aspect may explain the differences in results and conclusions between trials. In addition, the treadmill’s belt movement may impose the participant’s normal automatic reaction of gait, thus contributing to the differences observed between studies. Deterioration in postural control results from various mechanisms. It is well known that, to control balance, an accurate sensory integration of the vestibular, vision, and sensorimotor system is essential. It is possible that balance was sufficiently good with eyes open, so that there was little scope for the textured insoles to add to performance. However, removal of the visual system (eyes closed) may have increased independence on the sensorimotor system, allowing effects of textured insoles to become apparent. A similar observation has been previously reported in healthy older [16] and young [14] adults. We suggest an additional explanation for this finding. It is well known that mechanoreceptors respond to mechanical stimuli, including indentation and stretching of the skin. Mechanoreceptors can provide information as to texture, thereby enabling us to detect roughness, spacing, and orientation of textured patterns [33]. Consequently, the textured insole protrusions that are in direct contact with the plantar aspect of the foot cause a number of mechanoreceptors to react at a higher rate than with a smooth flat surface. Logically, people with MS who have balance deficits take advantage of the increased somatosensory information from the foot to maintain balance only when eyes are closed. This hypothesis is reinforced by previous reports examining the relationship among plantar sensation, vision
on gait [34], and postural control [15]. Meyer et al [15] demonstrated that, during static stance, statistically significant effects of foot-sole anesthesia on CoP were present only under eyes-closed conditions and included increases in CoP trajectories and sway rate. However, it is worth noting that, according to our plantar sensation results, this behavior does not modify sensory capabilities at the impairment level. Nevertheless, future studies are needed to clarify the exact contribution of the somatosensory information received from the sole of the foot for balance performance in people with MS.
Study Limitations This study has several limitations. A single type of textured insole was used. It is possible that a different texture pattern, in terms of geometric shape and distribution of indenting protrusions, would have produced different effects. In this context, balance performance was found to differ according to textured surface in elderly individuals [19]. In addition, the present study did not include a control group. There is a reasonable probability that the effects reported in the present study do not demonstrate any extra value over normal balance exercises. However, it would be of interest to investigate whether a combination of regular balance practice with textured insoles may display an advantage over regular balance practice alone in terms of balance and mobility. Finally, the sample size at follow-up was relatively small, which may have impeded the ability of this study to detect significant effects.
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Textured Insoles in MS
Conclusions This study found that textured insoles had no immediate effects or late effects on gait performance and plantar sensation. After 4 weeks of wear, there were improvements in some aspects of balance, specifically CoP path length and sway rate. However, it is unclear whether this was a placebo or learning effect. There is a possibility that, because the initial balance measurements were performed with no sensory insoles and only after with the sensory insoles, balance performance was influenced due to the initial experience. These preliminary data suggest the need for an in-depth investigation into the effects of prolonged wearing of textured insoles on gait and the effects on function in the MS population. Acknowledgments The authors thank Mrs. Phyllis Curchack Kornspan for editorial services. References 1. Cameron MH, Lord S. Postural control in multiple sclerosis: Implications for fall prevention. Curr Neurol Neurosci Rep 2010;10: 407-412. 2. Peterson EW, Cho CC, von Koch L, Finlayson ML. Injurious falls among middle aged and older adults with multiple sclerosis. Arch Phys Med Rehabil 2008;89:1031-1037. 3. Kalron A, Achiron A. Postural control, falls and fear of falling in people with multiple sclerosis without mobility aids. J Neurol Sci 2013;335:186-190. 4. Cattaneo D, Jonsdottir J, Zocchi M, Regola A. Effects of balance exercises on people with multiple sclerosis: A pilot study. Clin Rehabil 2007;21:771-781. 5. Stephens J, DuSchuttle D, Hatcher C, Shmunes J, Slaninka C. Use of awareness through movement improves balance and balance confidence in people with multiple sclerosis: A randomized controlled study. Neurol Report 2001;25:39-49. 6. Straudi S, Benedetti MG, Venturini E, Manca M, Foti C, Basaglia N. Does robot-assisted gait training ameliorate gait abnormalities in multiple sclerosis? A pilot randomized-control trial. NeuroRehabilitation 2013;33:555-563. 7. Jackson K, Edginton-Bigelow K, Cooper C, Merriman HA. Group kickboxing program for balance, mobility, and quality of life in individuals with multiple sclerosis: A pilot study. J Neurol Phys Ther 2012;36:131-137. 8. Guclu-Gunduz A, Citaker S, Irkec C, Nazliel B, Batur-Caglayan HZ. The effects of pilates on balance, mobility and strength in patients with multiple sclerosis. NeuroRehabilitation 2013;34:337342. 9. Bayraktar D, Guclu-Gunduz A, Yazici G, et al. Effects of Ai-Chi on balance, functional mobility, strength and fatigue in patients with multiple sclerosis: A pilot study. NeuroRehabilitation 2013;33:431437. 10. Nilsaga ˚rd YE, Forsberg AS, von Koch L. Balance exercise for persons with multiple sclerosis using Wii games: A randomised, controlled multi-centre study. Mult Scler 2013;19:209-216. 11. Romberg A, Virtanen A, Ruutiainen J, et al. Effects of a 6-month exercise program on patients with multiple sclerosis: A randomized study. Neurology 2004;63:2034-2038.
12. Lord S, Wade D, Halligan P. A comparison of two physiotherapy treatment approaches to improve walking in multiple sclerosis: A pilot randomized controlled study. Clin Rehabil 1998;12: 477-486. 13. Wiles C, Newcombe R, Fuller K, et al. Controlled randomised crossover trial of the effects of physiotherapy on mobility in chronic multiple sclerosis. J Neurol Neurosurg Psychiatry 2001;70: 174-179. 14. Cameron MH, Asano M, Bourdette D, Finlayson ML. People with multiple sclerosis use many fall prevention strategies but still fall frequently. Arch Phys Med Rehabil 2013;94: 1562-1566. 15. Meyer PF, Oddsson LI, De Luca CJ. The role of plantar cutaneous sensation on unperturbed stance. Exp Brain Res 2004;156: 505-512. 16. Kavounoudias A, Roll R, Roll JP. The plantar sole is a ’dynamometric map’ for human balance control. Neuroreport 1998;9: 3247-3252. 17. Corbin D, Hart J, McKeon P, Ingersoll C, Hertel J. The effect of textured insoles on postural control in double and single limb stance. J Sport Rehabil 2007;16:363-372. 18. Palluel E, Olivier I, Nougier V. The lasting effects of spike insoles on postural control in the elderly. Behav Neurosci 2009;123: 1141-1147. 19. Hatton A, Dixon J, Martin D, Rome K. Standing on textured surfaces: Effects on standing balance in healthy older adults. Age Ageing 2011;40:363-368. 20. Qiu F, Cole MH, Davids KW, et al. Enhanced somatosensory information decreases postural sway in older people. Gait Posture 2012;35:630-635. 21. Hatton AL, Dixon J, Martin D, Rome K. The effect of textured surfaces on postural stability and lower limb muscle activity. J Electromyogr Kinesiol 2009;19:957-964. 22. Hatton AL, Dixon J, Rome K, Newton JL, Martin DJ. Altering gait by way of stimulation of the plantar surface of the foot: The immediate effect of wearing textured insoles in older fallers. J Foot Ankle Res 2012;5:11. 23. Cameron MH, Horak FB, Herndon RR, Bourdette D. Imbalance in multiple sclerosis: A result of slowed spinal somatosensory conduction. Somatosens Mot Res 2008;25:113-122. 24. Kelleher KJ, Spence WD, Solomonidis S, Apatsidis D. The effect of textured insoles on gait patterns of people with multiple sclerosis. Gait Posture 2010;32:67-71. 25. Dixon J, Hatton AL, Robinson J, et al. Effect of textured insoles on balance and gait in people with multiple sclerosis: An explanatory trial. Physiotherapy 2014;100:142-149. 26. Polman CH, Reingold SC, Banwell B, et al. Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol 2011;69:292-302. 27. Bell-Krotoski J, Tomancik E. The repeatability of testing with Semmes-Weinstein monofilaments. J Hand Surg Am 1987;12:155161. 28. Dyck PJ, O’Brien PC, Kosanke JL, Gillen DA, Karnes JL. A 4, 2, and 1 stepping algorithm for quick and accurate estimation of cutaneous sensation threshold. Neurology 1993;43:1508-1512. 29. Faude O, Donath L, Roth R, Fricker L, Zahner L. Reliability of gait parameters during treadmill walking in community-dwelling healthy seniors. Gait Posture 2012;36:444-448. 30. Kalron A, Dvir Z, Frid L, Achiron A. Quantifying gait impairment using an instrumented treadmill in people with multiple sclerosis. ISRN Neurol 2013 Jun 25;2013:867575. 31. Properini L, Fortuna D, Gianni C, Leoardi L, Pozzilli C. The diagnostic accuracy of static posturography in predicting accidental falls in people with MS. Neurorehabil Neural Repair 2013; 27:45-52. 32. Prosperini L, Sbardella E, Raz E, et al. Multiple sclerosis: White and gray matter damage associated with balance deficit detected at static posturography. Radiology 2013;268:181-189.
A. Kalron et al. / PM R xx (2014) 1-9 33. Gardner E, Martin J. In: Kandel E, Schwartz J, Jessell T, eds. The Bodily Senses. In: Principles of Neural Science. New York: McGraw-Hill Health Professions Division; 2000; 412-430.
34. Perry SD, Santos LC, Palta AE. Contribution of vision and cutaneous sensation to the control of centre of mass (COM) during gait termination. Brain Res 2001;913:27-34.
Disclosure A.K. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel; and Department of Physical Therapy, Sackler Faculty of Medicine, Tel-Aviv University, Israel. Address correspondence to: A.K., st Habanim 60, Herzelia, Israel, 46379; e-mail: [email protected] Disclosure: nothing to disclose D.P. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel Disclosure: nothing to disclose
9
M.G.-A. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel Disclosure: nothing to disclose A.A. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel Disclosure: nothing to disclose Submitted for publication December 13, 2013; accepted August 12, 2014.
www.pmrjournal.org
Original Research
Do Textured Insoles Affect Postural Control and Spatiotemporal Parameters of Gait and Plantar Sensation in People With Multiple Sclerosis? Alon Kalron, PhD, Diana Pasitselsky, BPT, Michal Greenberg-Abrahami, MA, Anat Achiron, MD, PhD
Abstract Background: Balance and gait deficits are common in people with multiple sclerosis (MS). Physical interventions directed at improving balance and walking abilities have been implemented using various approaches. Nonetheless, no mode of training has been universally agreed upon. Objectives: To determine whether textured insoles have immediate effects on postural control and spatiotemporal parameters of gait and plantar sensation in people with people with MS and to explore effects 4 weeks after insole wear as to whether any immediate effects are maintained over time. Design: Within-subject experimental study with a 4-week intervention phase. Settings: Multiple Sclerosis Center, Center of Advanced Technologies in Rehabilitation, Sheba Medical Center, Tel-Hashomer, Israel. Participants: Twenty-five relapsing-remitting patients diagnosed with MS, 16 women and 9 men, aged 49.6 years (standard deviation ¼ 6.5 years). Intervention: Textured insoles customized according to foot size and adapted to the participant’s casual shoes. Main outcome measures: Spatiotemporal parameters of gait and center of pressure (CoP) excursions during static postural control were studied using the Zebris FDM-T Treadmill. Light-touch and pressure-sensation thresholds were determined using the Semmes-Weinstein monofilaments test. Results: Textured insoles did not alter static postural control parameters when examined with eyes open. Examination during the eyes-closed task demonstrated an immediate reduction in the CoP path length (298.4 mm, standard error ¼ 49.7 mm, versus 369.9 mm, SE ¼ 56.3 mm; P ¼.04) and sway rate (12.0 mm/s, standard error ¼ 1.4 mm/s, versus 15.1 mm/s, standard error ¼ 1.6 mm/s; P ¼ .03) after insertion of the textured insoles compared to casual shoes alone. These findings were maintained at termination of the insole 4-week intervention period. In terms of spatiotemporal parameters of gait, differences were not observed between casual shoes and shoes with textured insoles at baseline. Likewise, no differences were observed between initial and concluding gait trials. Significant differences in plantar sensitivity measures were not observed after the insole 4-week intervention phase. Conclusions: Although there were improvements in some aspects of balance, the efficacy of textured insoles in the MS population remains unclear.
Introduction Balance and gait deficits are common in people with multiple sclerosis (MS). These very disabling deficits reduce mobility and independence, lead to falls and injuries, and negatively affect quality of life [1-3]. In general, physical interventions directed at improving balance and walking abilities have implemented various approaches: for example, motor and sensory strategies [4], Feldenkrais exercises [5],
robot-assisted gait training [6], kickboxing [7], Pilates exercises [8], Ai-Chi exercises [9], Nintendo Wii games [10], strength and aerobic training [11], and neuromuscular facilitation [12,13]. Nevertheless, no mode of training has been universally agreed upon. Moreover, although PwMS use many fall prevention tactics, they nonetheless frequently fall [14]. Thus, additional types of intervention strategies aimed at improving balance and walking for people with MS should be considered.
1934-1482/$ - see front matter ª 2014 by the American Academy of Physical Medicine and Rehabilitation http://dx.doi.org/10.1016/j.pmrj.2014.08.942
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Textured Insoles in MS
It has been shown that feedback from plantar cutaneous afferents is important for the maintenance of normal balance when vision is inaccessible [15]. In addition, foot sole input contributes to the coding and the spatial representation of body posture [16]. Therefore, theoretically, wearing textured insoles can affect gait and balance by increased stimulation to the plantar surface of the feet, thereby influencing neuromuscular function. Several studies have reported that textured insoles reduce postural sway during standing in healthy young [17] and older [18-20] people. However, other studies have shown no clear benefit to healthy people [21] and older individuals who fall [22], during similar gait and balance tasks. It is well known that somatosensory deficit is a common feature of MS. Furthermore, previous trials have demonstrated that slowed spinal somatosensory conduction in people with MS while standing leads to extremely delayed postural responses [23]. Therefore, it is reasonable to consider textured insoles as an intervention alternative aimed at improving gait and balance abilities in people with MS. To date, there has been limited research as to the effects of textured insoles on mobility performance in the MS population [24,25]. According to our literature investigation, 2 studies examined this intervention strategy in PwMS. Kelleher et al, in a small study of 14 patients with MS, reported several effects on gait kinematics and kinetics, including benefits to knee and hip excursion, and ground reaction forces when wearing textured insoles constructed from sandpaper [24]. Conversely, no immediate effects were demonstrated in gait and balance performance in a group of 46 patients with MS who wore textured insoles. However, following a 2-week intervention phase of insole wear, improvements were observed in spatiotemporal parameters of gait [25], although it was unclear whether the response was a placebo or learning effect. It remains unclear as to whether textured insoles modify gait and balance performance and plantar sensation immediately and in the long term in people with MS. Given this knowledge, the purpose of the current study was 2-fold: (1) to determine whether textured insoles have immediate effects on postural control, spatiotemporal parameters of gait, and plantar sensation in people with MS; and (2) to explore effects 4 weeks after wearing the insoles as to whether any immediate effects are maintained over time.
were recruited from the Multiple Sclerosis Center, Sheba Medical Center, Tel-Hashomer, Israel. Inclusion criteria included a neurologist-confirmed diagnosis of definite relapsing-remitting MS according to the revised McDonald criteria [26]; the ability to walk without an assistive device (eg, a cane or walker); and relapse-free for at least 30 days before testing. Exclusion criteria included orthopedic disorders that could negatively affect mobility; major depression or cognitive decline; pregnancy; blurred vision; cardiovascular disorders; peripheral neuropathy; and diabetes. All patients were characterized by mobility difficulties confirmed by a neurological examination. Patients were then scored according to the Expanded Disability Status Scale (EDSS), an accepted method of quantifying disability in MS [24]. Ethical approval for the study was obtained by the Sheba Institutional Review Board. All participants signed an informed consent form. Textured Insoles Insoles were customized for both left and right feet according to the participant’s foot width and length. The insoles were 3 mm thick and made of elastic rubber and fabric. The coarse texture of the insole was designed with miniature square pyramids organized in a grid pattern (Figure 1). This material and design proved favorable, as it was considered sufficiently rough to provide sensory feedback, yet not rough enough to cause skin discomfort. Sensory Evaluation Light-touch and pressure-sensation thresholds were determined using the Semmes-Weinstein monofilaments test [27]. This measurement is a standardized test commonly used in research and sensory evaluation of peripheral and central nerve lesions and is usually used
Methods Study Participants This was a within-subject experimental study with a 4-week intervention phase. Twenty-five relapsingremitting patients diagnosed with MS, 16 women and 9 men, aged 49.6 years (standard deviation ¼ 6.5 years)
Figure 1. Insole designed with miniature square pyramids organized in a grid pattern.
A. Kalron et al. / PM R xx (2014) 1-9
as a criterion standard of touch-pressure threshold and tactile sensation. The sensory test was performed on 3 locations on the plantar surface of each foot: heel, medial forefoot, and lateral forefoot. A modified 4, 2, and 1 stepping algorithm [28] was used to evaluate the threshold point. The subjects lay prone, unable to observe the test procedure. The monofilaments test began with a size 4.17 filament. Depending on the subject’s response, the changes in stimulus intensity were executed in 3 increments until a change in their response was observed and a turnaround point reached. Changes were then made in 2 increments until another turnaround point, at which point all stimuli was presented into 1 increment. The tactile sensation threshold was determined as the lightest filament experienced >50% of the time. For each location tested, the examiner performed 2 null trials randomly placed throughout the algorithm. If the subject responded to both null trials at any given location, the test was halted and the subject reinstructed. Gait Analysis Spatiotemporal parameters of gait were studied using the Zebris FDM-T Treadmill (Zebris Medical GmbH, Germany). The Zebris FDM-T is fitted with an electronic mat of 10 240 miniature force sensors, each approximately 0.85 0.85 cm, embedded underneath the belt. The treadmill’s contact surface measures 150 50 cm, and its speed can be adjusted from 0.2 and 22 km/h, at intervals of 0.1 km/h. When the subject stands or walks on the treadmill, the force exerted by the feet (the socalled reactive-normal force in directions x, y, and z) is recorded by the sensors at a sampling rate of 120 Hz. Due to the high density of the sensors, the foot is mapped at a high resolution to facilitate even subtle changes in force distribution. Timing can also be monitored. Dedicated software integrates the force signals and provides 2-dimensional/3-dimensional graphic representation of major spatiotemporal parameters including center of pressure (CoP) trajectories during gait. In addition, we collected and analyzed the coefficient of variation (CV ¼ SD/mean) scores of step length and step time. The CV (%) is an acceptable relative measure of the intraindividual variability of spatiotemporal parameters of gait. The magnitude of the CV percentage corresponds to greater variability of the selected spatio-temporal parameter. Walking on an instrumented treadmill has several advantages compared to an over-ground device with similar footprint analysis capability. Specifically, compared to the electronic walkway, treadmill gait analysis is not limited to the number of steps per trial, thus enabling gait analysis over large distances. We assume that this ability is essential in the MS population because of fatigue concerns.
3
In 2012, Faude et al reported high levels of betweenand within-day reliability in healthy seniors for the majority of spatiotemporal gait parameters recorded by the Zebris Treadmill system during walking, with coefficients of variation typically less t han 5% and 7%, respectively [29]. Recently, the instrumented treadmill has been found to be an appropriate tool for assessing ambulation capabilities in people with MS. Furthermore, spatiotemporal gait parameters collected by this device during walking seem to be valid markers of neurological impairment in the MS population [30]. Static Postural Control Assessment Similar to gait analysis, static postural control parameters were obtained using the Zebris FDM-T Treadmill. A set of outcome measures taken from the CoP data during static stance were as follows: (1) ellipse sway area (mm2), defined as the 95% confidence ellipse for the mean of the CoP anterior, posterior, medial, and lateral coordinates; (2) CoP path length (mm), defined as the absolute length of the CoP path movements over the testing period; (3) sway rate (mm/s), defined as the mean speed of movement of the CoP during the testing period; and (4) average pressure distribution of the left and right foot expressed in bodyweight (%). Accordingly, the bilateral pressure distribution asymmetry score was calculated as the absolute difference in pressure distribution between legs. In a perfect symmetrical stance, this variable is 0. Experimental Design Upon acceptance into the study, each participant received a pair of textured insoles customized according to foot size and adapted to the participant’s casual shoes. The textured insoles were placed with the rigid texture in direct contact with the patient’s sole. Subsequently, the subjects completed a set of baseline measurements. Tests included sensory evaluation of both feet, followed by an examination of static postural control and gait. The last 2 examinations were carried out twice, wearing either casual shoes or casual shoes with the textured insoles. Before the treadmill gait measurement phase, all participants actively participated in an adaptationfamiliarization trial to establish the speed level of each individual. Starting at a fixed speed of 0.5 km/h, belt speed was increased by 0.3 km/h every 15 seconds, in a stepwise manner. When the participant informed the tester which speed best characterized that participant’s normal walking pace, that speed was designated as that individual’s comfort speed. After this adaptation phase, each participant was instructed to walk on the treadmill for 1 consecutive minute at the participant’s comfort speed. According to the participant’s
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Textured Insoles in MS
stride lengths, the amount of gait cycles included in the analysis ranged between 45 and 60. Posturography was carried out in the following manner. Each subject completed a sequence of 3 consecutive postural control tests under 3 different task conditions with a 1-minute break between tasks. Each task was repeated 3 times, for 20 seconds, followed by a 30-second rest period, as follows: (1) Eyes open: Subjects stood on the treadmill belt (10-cm gap between heels; 5 toe-out position), in an upright static position with arms resting at their sides. Participants were instructed to maintain their posture as steady as possible while visually focusing on a dot marked 1 m located directly in front of them. (2) Eyes closed: Conditions were identical to those of the eyes-open task but with eyes closed. (3) Narrowed base: Conditions were identical to those of the eyes-open task but with legs together. All measurements were performed at the Center of Advanced Technologies in Rehabilitation, Sheba Medical Center. Measurements were completed by an experienced physical therapist specialized in neurological rehabilitation. At termination of baseline measurements, textured insoles were provided. Participants were instructed to wear the textured insoles constantly throughout the day and to continue with their regular activities for 4 consecutive weeks. A physical therapist telephoned each person at the end of the first, second, and third week to detect possible difficulties or complaints encountered with the textured insoles. Re-assessment of standing balance, gait, and plantar sensation was completed after 4 weeks using the same procedures used at the first assessment. Statistical Analysis Descriptive statistics were performed to determine distributions of demographic, clinical, sensory, postural control, and gait parameters. All sensory and motor performance data were normally distributed according to the Kolmogorov-Smirnov test. The Spearman rho correlation analysis assessed the relationship between major postural control parameters to sensory evaluation measurements collected at baseline. Paired-samples t tests were performed to determine whether textured insoles had any immediate effects on postural control and spatiotemporal parameters of gait, and whether the 4-week intervention phase had any effects on postural control, spatiotemporal parameters of gait, and plantar sensation. Comparison between baseline and termination of the intervention program was based on measurements taken while wearing casual shoes without insoles. All analyses were performed using IBM SPSS statistics software (version 21.0 for Windows; IBM, Armonk, NY). All reported P values were 2 tailed. The level of significance was set at P < .05.
Table 1 Descriptive characteristics of study participants (n ¼ 25) Variable
Mean (SD)
Age, y Gender Male Female Ratio male/female Disease duration, y EDSS Pyramidal Cerebellar Visual Brainstem Cerebral Sensory
49.6 (6.5) 9 16 0.56 10.2 (7.5) 3.4 (3.0) 1.8 (1.0) 1.1 (1.0) 0.3 (0.5) 0.2 (0.5) 0.3 (0.5) 0.9 (1.0)
SD ¼ standard deviation; EDSS ¼ Expanded Disability Status Scale.
Results Descriptive characteristics of study participants are provided in Table 1. Significant Spearman rho correlation scores were shown between sensory evaluation measurements to the CoP path length and sway rate in the diverse condition tasks (eyes open, eyes closed, and legs together) (Table 2). These findings reinforce the main assumption of the present study that reduced plantar sensation is connected with poor balance control. The participants did not report any new neurological exacerbations during the experimental period. According to information obtained via telephone follow-up, no one asked to withdraw from the study. All participants reported that they had followed the study instructions regarding wearing of the textured insoles throughout the 4-week experimental period. Three patients reported mild disturbance related to insole wearing during the first week of the trial, but this resolved during the second week. Textured insoles did not alter static postural control parameters when examined with eyes open and at a narrowed base position. Static postural control parameters were also not altered at the immediate response phase and after the 4-week intervention. Nevertheless, examination during the eyes closed task demonstrated an immediate reduction in the CoP path length (298.4 mm, SE ¼ 49.7 mm, versus 369.9 mm, SE ¼ 56.3 mm; P ¼ .04) and sway rate (12.0 mm/s, SE ¼ 1.4 mm/s versus 15.1 mm/s, SE ¼ 1.6 mm/s, P ¼ .03) after insertion of textured insoles compared to wearing casual shoes without insoles. Moreover, these findings were maintained at termination of the insole 4-week intervention period. Static postural control performance at baseline is presented in Table 3. Postural control statistics after the 4-week insole intervention effects are presented in Table 4. In terms of mean and variability spatiotemporal parameters of gait, differences were not observed at
A. Kalron et al. / PM R xx (2014) 1-9
5
Table 2 Spearman rho correlation scores (P values) between sensory evaluation and major postural control parameters at baseline Task Condition
Open
Plantar Sensation Area
CoP
Sway Rate
CoP
Sway Rate
CoP
Sway Rate
.433 (.004) .513 (.001) .497 (.001)
.428 (.004) .516 (.001) .491 (.001)
.361 (.017) .311 (.043) .380 (.012)
.355 (.020) .308 (.045) .373 (.014)
.371 (.014) .421 (.027) .410 (.010)
.395 (.023) .368 (.005) .393 (.019)
.353 (.042) .574 (.001) .453 (.001)
.348 (.007) .573 (.001) .421 (.014)
.361 (.017) .430 (.004) .391 (.017)
.355 (.020) .426 (.004) .385 (.042)
.376 (.017) .330 (.034) .378 (.017)
.295 (.040) .429 (.035) .375 (.020)
Right Heel Medial forefoot Lateral forefoot Left Heel Medial forefoot Lateral forefoot
Closed
Legs Together
CoP ¼ center of pressure.
baseline between casual shoes and shoes with textured insoles. Likewise, no differences were observed between initial and concluding gait trials. Spatiotemporal gait outcomes in relationship to immediate wear of insoles (Table 5) and following the 4-week intervention period (Table 6) are presented. Significant differences in plantar sensitivity measures were not observed following the insole 4-week intervention phase. Sensory outcomes, defined by the Semmes-Weinstein monofilaments test at baseline and at termination of the intervention period were as follows: right heel (4.3, SE ¼ 0.2, versus 4.1 SE ¼ 0.3; P ¼ .60); right lateral forefoot (4.0, SE ¼ 0.2 versus 3.8, SE ¼ 0.2; P ¼ .38); right medial forefoot (4.0, SE ¼ 0.2, versus 4.1, SE ¼ 0.3); P ¼ .43); left heel (4.4, SE ¼ 0.2, versus 3.9, SE ¼ 0.2; P ¼ .34); left lateral forefoot (4.1, SE ¼ 0.3, versus 3.9, SE ¼ 0.2; P ¼ .51); and left medial forefoot (4.2, SE ¼ 0.2, versus 4.0, SE ¼ 0.2; P ¼ .61). Discussion The primary aim of the current study was to determine whether textured insoles affect postural control and gait in people with MS. Mobility parameters
were examined at 2 time points: immediately after wearing the insoles, and after a 4-week intervention period. Furthermore, we examined whether the 4-week intervention program altered plantar sensation. The underlying principle of the use of textured surfaces was to enhance sensory input. There is much debate relating to the effect of footwear on gait and postural control in various populations. According to our results, the efficacy of textured insoles remains unclear. Moreover, it is unclear whether textured insoles should be recommended for people with MS who have mobility impairments. On one hand, textured insoles had no effect on spatiotemporal parameters of gait, immediately and after the intervention period. Similar findings were observed with plantar sensation. Conversely, we found a reduction in several postural control variables, including CoP path length and sway rate performed with closed eyes, immediately and at termination of the insole intervention program. Importantly, these parameters have been found to correlate with balance performance and risk of falls in people with MS [3,31]. Recently, Prosperini et al found that, in people with MS, CoP trajectories measured during static stance were correlated with worse diffusion-tensor imaging parameters along the cerebellar
Table 3 Static postural control performance with shoes compared to shoes with insoles at baseline Mean (SE) Task Condition Eyes open
Eyes closed
Narrowed base
Postural Variable
Shoes 2
Ellipse sway area, mm CoP path length, mm Sway rate, mm/s Pressure distribution difference (%) Ellipse sway area, mm2 CoP path length, mm Sway rate, mm/s Pressure distribution difference, % Ellipse sway area, mm2 CoP path length, mm Sway rate, mm/s
SE ¼ standard error; CoP ¼ center of pressure. * P < .05.
165.4 256.1 12.9 9.6 267.1 369.9 15.1 12.0 198.9 309.9 15.5
(53.7) (45.4) (2.3) (1.4) (59.3) (56.3) (1.6) (1.8) (34.4) (31.5) (1.7)
Insoles
Mean Difference (SE)
P value
185.4 276.4 13.9 11.8 199.8 298.4 12.0 12.4 224.6 321.1 16.6
20.0 20.3 0.9 2.1 67.3 71.5 3.8 0.4 25.6 11.2 1.1
.50 .24 .29 .17 .12 .04* .03* .83 .25 .45 .24
(38.2) (35.2) (1.9) (2.0) (44.4) (49.7) (1.4) (2.5) (37.8) (35.1) (1.7)
(25.9) (16.8) (0.8) (1.5) (41.2) (32.3) (1.6) (1.6) (21.8) (14.7) (0.8)
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Textured Insoles in MS
Table 4 Static postural control performance at baseline and after the 4-week intervention period Mean (SE) Task Condition Eyes open
Eyes closed
Narrowed base
Postural Variable 2
Ellipse sway area (mm ) CoP path length (mm) Sway rate (mm/s) Pressure distribution difference (%) Ellipse sway area (mm2) CoP path length (mm) Sway rate (mm/s) Pressure distribution difference (%) Ellipse sway area (mm2) CoP path length (mm) Sway rate (mm/s)
Baseline
Post-intervention
Mean Difference (SE)
P value
165.4 256.1 12.9 9.6 267.1 369.9 15.1 12.0 198.9 309.9 15.5
148.8 242.0 12.3 11.4 162.7 302.1 12.3 11.2 181.6 312.5 15.9
16.8 14.1 0.6 1.8 104.4 67.8 2.8 0.8 17.3 2.6 0.4
.33 .25 .29 .46 .04* .03* .03* .39 .43 .78 .62
(53.7) (45.4) (2.3) (1.4) (59.3) (56.3) (1.6) (1.8) (34.4) (31.5) (1.7)
(38.3) (39.5) (2.0) (2.7) (32.9) (42.3) (1.2) (2.1) (29.6) (30.7) (1.6)
(22.3) (12.7) (0.7) (1.9) (31.6) (28.7) (1.1) (1.0) (22.7) (15.1) (1.4)
SE ¼ standard error; CoP ¼ center of pressure. * P < .05.
connections and supratentorial associative white matter bundles. Gray matter atrophy of the superior lobules of the cerebellum (IV, V, VI) and lobules VIII also correlated with worse posturometric values [32]. Nevertheless, no changes in postural control were observed when examined with eyes open. To the best of the authors’ knowledge, no more than 2 studies have explored the efficacy of footwear intervention on gait and balance in the MS population [24,25]. Although there are differences between our and previous studies, mainly in terms of study design and outcome measures, we found the comparison worth discussing. Dixon et al [25] reported that textured insoles had no significant immediate effect on gait variables compared with control conditions. However, they reported that after the 2-week intervention period, the insole intervention group demonstrated an increase in step and stride length. In contrast, the
current study data did not attest to significant changes in 14 (of 14) spatiotemporal parameters of gait after the 4-week intervention phase. We assume that the different measurement devices between our study and that of Dixon et al may have been the cause of this dissimilarity. Whereas Dixon et al [25] measured over-ground gait using an electronic walkway, we collected spatiotemporal parameters of gait with an instrumented treadmill. The main difference between measurement procedures relates to control of the participants’ walking speed. The instrumented treadmill enables the examiner to control velocity of gait. Accordingly, in the present study, speed of walking was defined at baseline and was preset for all other gait trials, including at the completion of the intervention program. In contrast, control of speed with over-ground measurement equipment is not possible; that is, speed of
Table 5 Spatiotemporal gait outcomes with shoes compared to shoes with insoles at baseline Mean (SE) Gait Variable
Shoes
Insoles
Mean Difference (SE)
P value
Velocity, km/h Cadence, steps/min Step time R, s Step time L, s CV step time R, % CV step time L, % Step length R, cm Step length L, cm CV step time R, % CV step time L, % Stance R, % GC Stance L, % GC Single support R, % GC Single support L, % GC Double support, % GC Stride time, s Stride length, cm Step width, cm
2.5 96.7 0.63 0.63 3.6 3.4 42.9 42.8 3.5 3.8 69.0 68.9 31.1 31.0 37.9 1.26 85.7 11.7
2.5 95.7 0.65 0.66 3.7 3.2 41.4 41.5 3.4 3.7 69.3 68.7 31.3 30.7 38.0 1.30 82.9 11.3
0.005 1.0 0.02 0.03 0.1 0.2 1.5 1.3 0.1 0.1 0.3 0.2 0.2 0.3 0.1 0.04 2.8 0.4
.45 .19 .38 .27 .86 .74 .43 .21 .56 .78 .12 .12 .18 .21 .22 .07 .09 .24
(0.2) (2.7) (0.02) (0.02) (2.1) (2.8) (3.2) (3.1) (2.3) (2.2) (0.8) (1.0) (1.0) (0.8) (1.7) (0.03) (6.2) (0.7)
(0.2) (3.3) (0.03) (0.03) (2.4) (1.9) (2.7) (2.7) (2.7) (2.1) (0.7) (0.8) (1.6) (0.7) (1.5) (0.05) (5.4) (0.7)
SE ¼ standard error; R ¼ Right; L ¼ Left; CV ¼ coefficient of variation; GC ¼ gait cycle.
(0.1) (0.9) (0.09) (0.09) (1.3) (1.5) (2.0) (1.1) (1.4) (1.3) (0.6) (0.6) (0.8) (0.8) (1.0) (0.02) (4.1) (0.3)
A. Kalron et al. / PM R xx (2014) 1-9
7
Table 6 Spatiotemporal gait outcomes at baseline and after the 4-week intervention period Mean (SE) Gait Variable
Baseline
Post-intervention
Mean Difference (SE)
P value
Velocity, km/h Cadence, steps/min Step time R, sec Step time L, sec CV step time R, % CV step time L, % Step length R, cm Step length L, cm CV step time R, % CV step time L, % Stance R, % GC Stance L, % GC Single support R, % GC Single support L, % GC Double support, % GC Stride time, s Stride length, cm Step width, cm
2.5 96.7 0.63 0.63 3.6 3.4 42.9 42.8 3.5 3.8 69.0 68.9 31.1 31.0 37.9 1.26 85.7 11.7
2.5 100.2 0.61 0.62 3.3 3.2 41.5 41.2 3.6 3.7 69.3 68.6 31.4 30.7 37.9 1.23 82.8 11.3
0.005 3.5 0.02 0.001 0.3 0.2 1.4 1.5 0.1 0.1 0.3 0.3 0.3 0.3 0.03 0.03 2.9 0.4
.98 .21 .26 .66 .45 .59 .60 .58 .88 .69 .66 .62 .60 .71 .98 .44 .59 .27
(0.2) (2.7) (0.02) (0.02) (2.1) (2.8) (3.2) (3.1) (2.3) (2.2) (0.8) (1.0) (1.0) (0.8) (1.7) (0.03) (6.2) (0.7)
(0.3) (3.3) (0.02) (0.03) (2.3) (2.7) (3.4) (3.6) (2.9) (2.2) (1.0) (1.0) (1.0) (1.0) (2.0) (0.05) (7.0) (0.7)
(0.16) (2.7) (0.02) (0.09) (1.9) (1.8) (2.5) (2.7) (2.1) (1.8) (0.7) (0.6) (0.6) (0.7) (1.3) (0.04) (5.2) (0.4)
SE ¼ standard error; R ¼ right; L ¼ left; CV ¼ coefficient of variation; GC ¼ gait cycle.
walking is independent for each gait test. The differences in the speed control aspect may explain the differences in results and conclusions between trials. In addition, the treadmill’s belt movement may impose the participant’s normal automatic reaction of gait, thus contributing to the differences observed between studies. Deterioration in postural control results from various mechanisms. It is well known that, to control balance, an accurate sensory integration of the vestibular, vision, and sensorimotor system is essential. It is possible that balance was sufficiently good with eyes open, so that there was little scope for the textured insoles to add to performance. However, removal of the visual system (eyes closed) may have increased independence on the sensorimotor system, allowing effects of textured insoles to become apparent. A similar observation has been previously reported in healthy older [16] and young [14] adults. We suggest an additional explanation for this finding. It is well known that mechanoreceptors respond to mechanical stimuli, including indentation and stretching of the skin. Mechanoreceptors can provide information as to texture, thereby enabling us to detect roughness, spacing, and orientation of textured patterns [33]. Consequently, the textured insole protrusions that are in direct contact with the plantar aspect of the foot cause a number of mechanoreceptors to react at a higher rate than with a smooth flat surface. Logically, people with MS who have balance deficits take advantage of the increased somatosensory information from the foot to maintain balance only when eyes are closed. This hypothesis is reinforced by previous reports examining the relationship among plantar sensation, vision
on gait [34], and postural control [15]. Meyer et al [15] demonstrated that, during static stance, statistically significant effects of foot-sole anesthesia on CoP were present only under eyes-closed conditions and included increases in CoP trajectories and sway rate. However, it is worth noting that, according to our plantar sensation results, this behavior does not modify sensory capabilities at the impairment level. Nevertheless, future studies are needed to clarify the exact contribution of the somatosensory information received from the sole of the foot for balance performance in people with MS.
Study Limitations This study has several limitations. A single type of textured insole was used. It is possible that a different texture pattern, in terms of geometric shape and distribution of indenting protrusions, would have produced different effects. In this context, balance performance was found to differ according to textured surface in elderly individuals [19]. In addition, the present study did not include a control group. There is a reasonable probability that the effects reported in the present study do not demonstrate any extra value over normal balance exercises. However, it would be of interest to investigate whether a combination of regular balance practice with textured insoles may display an advantage over regular balance practice alone in terms of balance and mobility. Finally, the sample size at follow-up was relatively small, which may have impeded the ability of this study to detect significant effects.
8
Textured Insoles in MS
Conclusions This study found that textured insoles had no immediate effects or late effects on gait performance and plantar sensation. After 4 weeks of wear, there were improvements in some aspects of balance, specifically CoP path length and sway rate. However, it is unclear whether this was a placebo or learning effect. There is a possibility that, because the initial balance measurements were performed with no sensory insoles and only after with the sensory insoles, balance performance was influenced due to the initial experience. These preliminary data suggest the need for an in-depth investigation into the effects of prolonged wearing of textured insoles on gait and the effects on function in the MS population. Acknowledgments The authors thank Mrs. Phyllis Curchack Kornspan for editorial services. References 1. Cameron MH, Lord S. Postural control in multiple sclerosis: Implications for fall prevention. Curr Neurol Neurosci Rep 2010;10: 407-412. 2. Peterson EW, Cho CC, von Koch L, Finlayson ML. Injurious falls among middle aged and older adults with multiple sclerosis. Arch Phys Med Rehabil 2008;89:1031-1037. 3. Kalron A, Achiron A. Postural control, falls and fear of falling in people with multiple sclerosis without mobility aids. J Neurol Sci 2013;335:186-190. 4. Cattaneo D, Jonsdottir J, Zocchi M, Regola A. Effects of balance exercises on people with multiple sclerosis: A pilot study. Clin Rehabil 2007;21:771-781. 5. Stephens J, DuSchuttle D, Hatcher C, Shmunes J, Slaninka C. Use of awareness through movement improves balance and balance confidence in people with multiple sclerosis: A randomized controlled study. Neurol Report 2001;25:39-49. 6. Straudi S, Benedetti MG, Venturini E, Manca M, Foti C, Basaglia N. Does robot-assisted gait training ameliorate gait abnormalities in multiple sclerosis? A pilot randomized-control trial. NeuroRehabilitation 2013;33:555-563. 7. Jackson K, Edginton-Bigelow K, Cooper C, Merriman HA. Group kickboxing program for balance, mobility, and quality of life in individuals with multiple sclerosis: A pilot study. J Neurol Phys Ther 2012;36:131-137. 8. Guclu-Gunduz A, Citaker S, Irkec C, Nazliel B, Batur-Caglayan HZ. The effects of pilates on balance, mobility and strength in patients with multiple sclerosis. NeuroRehabilitation 2013;34:337342. 9. Bayraktar D, Guclu-Gunduz A, Yazici G, et al. Effects of Ai-Chi on balance, functional mobility, strength and fatigue in patients with multiple sclerosis: A pilot study. NeuroRehabilitation 2013;33:431437. 10. Nilsaga ˚rd YE, Forsberg AS, von Koch L. Balance exercise for persons with multiple sclerosis using Wii games: A randomised, controlled multi-centre study. Mult Scler 2013;19:209-216. 11. Romberg A, Virtanen A, Ruutiainen J, et al. Effects of a 6-month exercise program on patients with multiple sclerosis: A randomized study. Neurology 2004;63:2034-2038.
12. Lord S, Wade D, Halligan P. A comparison of two physiotherapy treatment approaches to improve walking in multiple sclerosis: A pilot randomized controlled study. Clin Rehabil 1998;12: 477-486. 13. Wiles C, Newcombe R, Fuller K, et al. Controlled randomised crossover trial of the effects of physiotherapy on mobility in chronic multiple sclerosis. J Neurol Neurosurg Psychiatry 2001;70: 174-179. 14. Cameron MH, Asano M, Bourdette D, Finlayson ML. People with multiple sclerosis use many fall prevention strategies but still fall frequently. Arch Phys Med Rehabil 2013;94: 1562-1566. 15. Meyer PF, Oddsson LI, De Luca CJ. The role of plantar cutaneous sensation on unperturbed stance. Exp Brain Res 2004;156: 505-512. 16. Kavounoudias A, Roll R, Roll JP. The plantar sole is a ’dynamometric map’ for human balance control. Neuroreport 1998;9: 3247-3252. 17. Corbin D, Hart J, McKeon P, Ingersoll C, Hertel J. The effect of textured insoles on postural control in double and single limb stance. J Sport Rehabil 2007;16:363-372. 18. Palluel E, Olivier I, Nougier V. The lasting effects of spike insoles on postural control in the elderly. Behav Neurosci 2009;123: 1141-1147. 19. Hatton A, Dixon J, Martin D, Rome K. Standing on textured surfaces: Effects on standing balance in healthy older adults. Age Ageing 2011;40:363-368. 20. Qiu F, Cole MH, Davids KW, et al. Enhanced somatosensory information decreases postural sway in older people. Gait Posture 2012;35:630-635. 21. Hatton AL, Dixon J, Martin D, Rome K. The effect of textured surfaces on postural stability and lower limb muscle activity. J Electromyogr Kinesiol 2009;19:957-964. 22. Hatton AL, Dixon J, Rome K, Newton JL, Martin DJ. Altering gait by way of stimulation of the plantar surface of the foot: The immediate effect of wearing textured insoles in older fallers. J Foot Ankle Res 2012;5:11. 23. Cameron MH, Horak FB, Herndon RR, Bourdette D. Imbalance in multiple sclerosis: A result of slowed spinal somatosensory conduction. Somatosens Mot Res 2008;25:113-122. 24. Kelleher KJ, Spence WD, Solomonidis S, Apatsidis D. The effect of textured insoles on gait patterns of people with multiple sclerosis. Gait Posture 2010;32:67-71. 25. Dixon J, Hatton AL, Robinson J, et al. Effect of textured insoles on balance and gait in people with multiple sclerosis: An explanatory trial. Physiotherapy 2014;100:142-149. 26. Polman CH, Reingold SC, Banwell B, et al. Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol 2011;69:292-302. 27. Bell-Krotoski J, Tomancik E. The repeatability of testing with Semmes-Weinstein monofilaments. J Hand Surg Am 1987;12:155161. 28. Dyck PJ, O’Brien PC, Kosanke JL, Gillen DA, Karnes JL. A 4, 2, and 1 stepping algorithm for quick and accurate estimation of cutaneous sensation threshold. Neurology 1993;43:1508-1512. 29. Faude O, Donath L, Roth R, Fricker L, Zahner L. Reliability of gait parameters during treadmill walking in community-dwelling healthy seniors. Gait Posture 2012;36:444-448. 30. Kalron A, Dvir Z, Frid L, Achiron A. Quantifying gait impairment using an instrumented treadmill in people with multiple sclerosis. ISRN Neurol 2013 Jun 25;2013:867575. 31. Properini L, Fortuna D, Gianni C, Leoardi L, Pozzilli C. The diagnostic accuracy of static posturography in predicting accidental falls in people with MS. Neurorehabil Neural Repair 2013; 27:45-52. 32. Prosperini L, Sbardella E, Raz E, et al. Multiple sclerosis: White and gray matter damage associated with balance deficit detected at static posturography. Radiology 2013;268:181-189.
A. Kalron et al. / PM R xx (2014) 1-9 33. Gardner E, Martin J. In: Kandel E, Schwartz J, Jessell T, eds. The Bodily Senses. In: Principles of Neural Science. New York: McGraw-Hill Health Professions Division; 2000; 412-430.
34. Perry SD, Santos LC, Palta AE. Contribution of vision and cutaneous sensation to the control of centre of mass (COM) during gait termination. Brain Res 2001;913:27-34.
Disclosure A.K. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel; and Department of Physical Therapy, Sackler Faculty of Medicine, Tel-Aviv University, Israel. Address correspondence to: A.K., st Habanim 60, Herzelia, Israel, 46379; e-mail: [email protected] Disclosure: nothing to disclose D.P. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel Disclosure: nothing to disclose
9
M.G.-A. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel Disclosure: nothing to disclose A.A. Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel Disclosure: nothing to disclose Submitted for publication December 13, 2013; accepted August 12, 2014.
