http://informahealthcare.com/idt ISSN 1748-3107 print/ISSN 1748-3115 online Disabil Rehabil Assist Technol, Early Online: 1–6 ! 2015 Informa UK Ltd. DOI: 10.3109/17483107.2015.1027296
RESEARCH PAPER
The impact of walking speed on the effects of functional electrical stimulation for foot drop in people with multiple sclerosis Disabil Rehabil Assist Technol Downloaded from informahealthcare.com by Fudan University on 05/10/15 For personal use only.
L. Miller1,2, D. Rafferty2, L. Paul3, and P. Mattison1 1
MS Service, NHS Ayrshire and Arran, Scotland, UK, 2School of Health and Life Sciences, Glasgow Caledonian University, Glasgow, Scotland, UK, and School of Medicine, University of Glasgow, Glasgow, Scotland, UK
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Abstract
Keywords
Purpose: Functional electrical stimulation (FES) is effective in assisting people with multiple sclerosis (pwMS) with gait. Previous studies have investigated the effects of FES in pwMS with slow self-selected walking speeds (SSWS). This study reports on the effect of the Odstock Dropped Foot Stimulator (ODFS) on the speed and oxygen (O2) cost of gait in pwMS walking at a range of SSWS. Methods: Twenty pwMS (mean age 50.4 ± 7.3 years) currently using FES walked at their SSWS for 5 min with and without FES. O2 cost of gait was measured using a gas analysis system, and gait speed was calculated. Data were analysed for all participants, and comparisons were made between those with a SSWS5and40.8 m/s (walking speed required for community ambulation). Results: Significant improvements in the speed and O2 cost of gait were seen using FES in the group with SSWS 50.8 m/s (n ¼ 11, p ¼ 0.005). When participants’ SSWS 40.8 m/s, no difference in gait speed was noted, and a significant increase in O2 cost of gait using FES (n ¼ 9, p ¼ 0.004) was noted. Conclusion: FES has a different effect on the speed and O2 cost of gait dependent on the SSWS of pwMS. This requires further investigation.
Functional electrical stimulation, gait speed, walking History Received 10 August 2014 Revised 23 December 2014 Accepted 5 March 2015 Published online 31 March 2015
ä Implications for Rehabilitation
Functional electrical stimulation (FES) used for foot drop is effective in improving the speed and oxygen cost of walking in pwMS walking at SSWS 50.8 m/s. FES does not seem to have a beneficial effect on the speed and oxygen cost of walking in pwMS walking at SSWS 40.8 m/s. Further research is needed to understand the possible mechanisms involved so that FES for foot drop can be efficiently prescribed.
Introduction In multiple sclerosis (MS), a common neurological condition affecting young adults, walking impairment impacting on disability and participation occurs in around 75% of this population [1–3]. Functional electrical stimulation (FES) is an assistive technology with great potential for restoring movement [4]. When used for foot drop, it is designed to enhance mobility in the home and community. The ability to walk around independently within ones community or ‘‘community ambulation’’ is defined as outdoor walking encompassing activities such as visits to the supermarket, bank or shops, social outings and leisure activities [5]. There is a strong correlation between walking speed and community ambulation in people with multiple sclerosis (pwMS), with selfselected walking speeds (SSWS) of 0.79 m/s being found to be a good indicator of community ambulation [6]. Gait speeds of 0.8 m/s have also been found to be reliable measures of Address for correspondence: L. Miller, School of Health and Life Sciences, Glasgow Caledonian University, Glasgow G40BA, Scotland, UK. E-mail: [email protected]
community ambulation and improved participation in stroke patients [7]. Weakness and fatigue in ankle dorsiflexors contribute to foot drop and impacting on gait in MS. Higher levels of fatigue, increased effort and slower walking speeds have been reported in people with MS, compared to healthy controls [8,9]. FES is used to treat foot drop, and by stimulating the common peroneal nerve via skin surface electrodes the resulting ankle dorsiflexion helps to aid foot clearance. In addition, the stimulation may inhibit antagonists such as the calf muscles and assist flexion at other joints through a flexor withdrawal reflex [10]. FES facilitates a more natural gait pattern, increases circulation and reduces muscle atrophy [11]. There is evidence of an ‘‘orthotic’’ effect of FES on walking in MS and other central nervous system (CNS) disorders [11–19]. An orthotic effect is seen when an individual walks with FES in comparison to walking without FES. Orthotic effects of FES have been noted in pwMS with regards to walking distance and endurance [12], speed and the Physiological Cost Index (PCI) of gait [13–17], oxygen (O2) cost of gait [16,19], falls and occupational performance [17]. Lord et al. [5] suggest that rehabilitation efforts need to be focused to achieve a level of
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mobility sufficient for community ambulation. Previous studies have investigated the effects of FES in pwMS with slow selfselected walking speeds (SSWS) [11,15] and noted significant improvements towards achieving speeds required for community ambulation. There have been no studies reporting the effects of FES in pwMS walking at SSWS 40.8 m/s. There is a need to examine the impact of FES in this group of people with MS in order to determine if there are benefits, so that treatment can be targeted effectively. This paper reports on the effects of the Odstock Foot Drop Stimulator (ODFS), a type of FES device which uses a pressure switch in the heel of the shoe. Previous results from this study which also compared two different types of FES have been previously reported [19]. This study aims to investigate the effect of FES on the speed and O2 cost of gait in pwMS walking at SSWS of 4 and 50.8 m/s.
Materials and methods Ethics Ethics approval was granted from the West of Scotland Research Ethics Committee. NHS Ayrshire and Arran sponsored the study. Subjects The lead clinician identified 56 potential participants with MS from the FES database of NHS Ayrshire and Arran, who met the inclusion/exclusion criteria. They sent the participant information leaflet inviting them to participate in the study. To be included in the study, participants had to: have used ODFS III FES device (OML, Salisbury, UK) for 6 months or more, be able to walk continuously for 5 min and score between 2 (abnormal gait or episodic imbalance; gait disorder is noticed by family and friends; able to walk 25 feet in 10 s or less) and 6 (requires bilateral support and more than 20 s to walk 25 feet; may use wheelchair on occasion) on the Hauser Ambulation Index (HAI) [20]. Potential participants were excluded if they had a recent relapse (within the previous six weeks) or suffered from other neurological disease or co-morbidities restricting gait. Twenty four participants agreed to participate and gave written, informed consent.
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analysis system was fitted to the participants, ensuring the facemask (Hans Rudolph Inc, Kansas City, MO) was comfortable but tight enough to prevent leakage. Gas analysis started 2 min prior to, and continued 2 min after, each walking test. The percentage of expired O2 during over ground gait was used to calculate the O2 cost of gait. This protocol has been previously used by the authors [16,19]. Previous validation of the COSMED system has been undertaken, which found to be acceptable for measuring oxygen uptake in healthy adults over a range of exercise intensities [20]. Test–retest reliability of the oxygen measures for the K4 has been found to be good in healthy adults [21]; however, there has been no previous work in MS. Good to excellent ICC’s have been reported and supports using single point in time measures for this measure [21]. Although there has been no previous validation or reliability of the SSWS in MS, the 6-min walk test has been found to have excellent intra-rater reliability (ICC ¼ 0.950) [22]. Data analysis Descriptive statistics for demographics and baseline variables are presented as means and standard deviations and include; age, time since diagnosis, Hauser Ambulation Index [23], time since using FES. Distance and duration of the walk were recorded. O2 uptake per kilogram body weight (ml/min/kg) and the O2 cost [i.e. physiological cost per unit distance walked (VO2/speed of gait) (ml/min/kg/m)] [24] were recorded and used to analyse the O2 cost of gait during the two conditions. The average of these parameters was calculated using data between minutes 3 and 4 of the walking test when a steady state is achieved [25]. Paired t tests were used to investigate the difference between walking with and without FES with respect to gait speed, O2 uptake and O2 cost of gait. The participants were split into two groups based on their self-selected gait speed (without FES) using the cut off point of 0.8 m/s which defines the walking speed required for community ambulation [9]. A paired t test was used to compare gait speed, O2 uptake and O2 cost of gait with and without FES within each of the groups. The level of significance was set at p50.05, and analysis was performed on Minitab v15 (Coventry, UK).
Procedure The Odstock Dropped Foot Stimulator III (ODFS III) (OML, Salisbury, UK) FES device was used. The ODFS III uses a foot switch placed in the heel of the shoe which detects heel contact and synchronises stimulation of tibialis anterior at heel raise during the swing phase of walking. Before beginning the testing procedure, the ODFS III was checked by a neurophysiotherapist experienced in the application of FES to ensure settings, and electrode position was optimal. A stimulation frequency of 40 Hz was used to stimulate the common peroneal nerve, and the optimal contraction strength was achieved by adjusting the output intensity and the pulse width (3–350 ms). Waveform, ramps and the extension period had been previously optimised to suit each participants gait style and speed. Participants attended on one occasion only and walked on a level floor at their SSWS for 5 min around an elliptical course outlined by two cones 9.5 m apart, giving a 10-m shuttle length. The participants walked once with FES and once without FES with the order of testing being randomised. Participants rested for a minimum of 5 min between tests. A COSMED K4b2 (Cosmed, Rome, Italy) gas analysis system was used to measure the percentage of expired oxygen during over-ground gait. The COSMED system was calibrated prior to each session according to manufacturer’s instructions. Gait speed was calculated by measuring the total distance travelled during each 5 minute walk using a lap counter, tape measure and standard stopwatch. The gas
Results Demographics Of the 24 participants included, four sets of data were excluded from the analysis due to poor fit of face mask resulting in inaccuarte O2 uptake readings(n ¼ 2) and inability of the participant to complete the protocol (n ¼ 2). Table 1 presents the demographics of the remaining participants (n ¼ 20). The mean age was 50.4 ± 7.3 years, time since diagnosis was 11.2 ± 8.6 years, and the HAI score was 4 ± 2.75. The majority of the participants had Relapsing Remitting (RR) MS, and there were equal numbers of males and females. The participants were split into two groups based on their SSWS (without FES), those who walked at SSWS of 50.8 m/s and those who walked at SSWS 40.8 m/s. The group who walked at slower SSWS (50.8 m/s) had significantly greater mean Extended Disability Status Score (EDSS), and Hauser Ambulation Index (HAI) scores were older and had used FES for longer compared to the group who walked at SSWS 40.8 m/s (all p50.01) (Table 1). Orthotic effect of FES on walking speed, O2 uptake and O2 cost of walking Considering all participants (n ¼ 20), pwMS walked significantly faster using FES compared to without (p ¼ 0.043) (Table 2). There were no differences in O2 uptake (p ¼ 0.109) or the O2 cost
Impact of walking speed on FES in MS
DOI: 10.3109/17483107.2015.1027296
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Table 1. Demographics: age, mass, height, body mass index (BMI), time since diagnosis (TSD), Extended Disability Status Scale (EDSS), Hauser Ambulation Index (HAI) and time using FES (tFES) of all participants (n ¼ 20), participants who walked at speeds of50.8 m/s (n ¼ 11) and participants who walked at speeds of 40.8 m/s (n ¼ 9). Group All (n ¼ 20) 50.8 m/s (n ¼ 11) 40.8 m/s (n ¼ 9) p
Age (years)
Mass (kg)
Height (cm)
BMI (kg/m2)
TSD
EDSSa
HAIa
tFESa (years)
50.4 (7.3) 54.2 (7.1) 46.6 (4.5) 40.01
80.4 (20.4) 85.6 (22.5) 74 (16.5) NS
169 (9.5) 170 (8.1) 166 (11.1) NS
28 (5.4) 29.3 (6.3) 26.5 (3.8) NS
11.2 (8.6) 13.1 (8.8) 8.9 (8.2) NS
5.3 (2) 6 (0) 4 (1.5) 40.01
4 (2.75) 5 (2) 2 (1.5) 40.01
2 (5.75) 6 (6) 1 (0.5) 40.01
One-way ANOVA was used to compare groups. Data are reported as means and standard deviations but where data not normally distributed. Values are reported as medians and (IQRs).
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Table 2. Mean walking speed (m/s), O2 uptake (ml/min/kg) and O2 cost (VO2) with and without FES in all participants (n ¼ 20), pwMS who walked 50.8 m/s (n ¼ 11) and pwMS who walked 40.8 m/s (n ¼ 9). Condition
All data (n ¼ 20) Speed (m/s) VO2 (ml/min/kg) Oxygen cost (ml/min/kg/m) pwMS walk 50.8 m/s (n ¼ 11) Speed (m/s) VO2 (ml/min/kg) Oxygen cost (ml/min/kg/m/) pwMS walk 40.8 m/s (n ¼ 9) Speed (m/s) VO2 (ml/min/kg) Oxygen cost (ml/min/kg/m)
NO FES
ODFS
Post-hoc testing
0.69 (0.31) 11.96 (3.0) 0.36 (0.20)
0.73 (0.28) 12.50 (2.71) 0.33 (0.16)
0.043 0.109 0.120
0.46 (0.18) 11.70 (2.40) 0.48 (0.19)
0.53 (0.17) 11.96 (1.35) 0.41 (0.16)
0.005 0.688 0.020
0.97 (0.15) 12.17 (3.76) 0.21 (0.07)
0.97 (0.18) 13.17 (3.77) 0.24 (0.08)
0.744 0.084 0.004
of gait (p ¼ 0.120) when walking with FES in comparison to without FES. The effects of FES on gait in pwMS walking at SSWS 50.8 m/s Participants in the group who walked at SSWS 50.8 m/s had an average gait speed of 0.46 m/s (±0.18) without FES and 0.53 m/s (±0.17) with FES (p ¼ 0.005). There was also a significant reduction in O2 cost of gait with FES in comparison to without (p ¼ 0.02) (Table 2). The effect of FES on gait in pwMS walking at SSWS 40.8 m/s Participants who walked at SSWS 40.8 m/s on average walked at a similar speed with FES (0.97 ± 0.18 m/s) in comparison to without FES (0.97 ± 0.15 m/s) (p ¼ 0.74). There was a nonsignificant increase in O2 uptake (p ¼ 0.84) and a statistically significant increase in O2 cost of walking (p ¼ 0.004) with FES in comparison to without (Table 2). The different effects of FES noted on gait speed, O2 uptake and O2 cost of gait in participants walking at SSWS 40.8 m/s in comparison to those 50.8 m/s are presented in Figure 1 (a–f).
Discussion This study found that walking speed significantly improved with FES compared to without in this cohort of pwMS. FES, however, had a different effect on the speed and O2 cost of gait which was dependent on SSWS. There were significant improvements in the speed and a reduction in O2 cost of gait in those with a SSWS
50.8 m/s, however, those with a SSWS 40.8 m/s demonstrated no improvement in speed and an increase in the O2 cost of gait. This study has confirmed the findings of previous studies in MS [12,16,19] where significant orthotic effects of FES on walking speed have been found. The failure to demonstrate significant improvements in the O2 cost of walking was in contrast to our earlier study using the same protocol [16]. This is the first FES study in MS which has recruited pwMS across a spectrum of disability levels resulting in heterogeneity in the SSWS’s of participants. The participants presented with walking speeds that ranged from 0.21 to 1.23 m/s with a mean walking speed of 0.69 ± 0.31 m/s without FES. Our earlier study [16] evaluated the effect of FES in pwMS who walked at a mean SSWS of 0.43 ± 0.15 m/s, and none of the participants walked at speeds of greater than 0.8 m/s. The current study aimed to recruit participants across a range of disability levels presenting with foot drop which resulted in a number of participants (n ¼ 9) walking at SSWS40.8 m/s. The recruitment of a more heterogeneous sample may have contributed towards a smaller increase in walking speed and the failure to demonstrate a significant reduction in the O2 cost of walking. The greatest benefits from FES in terms of the speed and energy cost of walking were seen in the group who walked at SSWS 50.8 m/s. Weiler et al. [26] had also previously noted that the largest relative gains in walking speed were seen in slower walkers (speeds of 50.3 m/s) in spinal cord injury (SCI) and stroke participants using FES. This, however, has not been previously demonstrated within MS. Barrett et al. [12] suggested that those with MS presenting with lower limb muscle weakness may benefit to a greater extent from the strengthening and reeducation effects of FES than those without muscle weakness. There is also evidence of a positive effect of FES on lower limb spasticity [27] which is more likely to be a symptom for pwMS walking at slower speeds (40.8 m/s). Sosnoff et al. [28] found that pwMS presenting with spasticity in the gastrocnemius and soleus muscles had greater disability, walked slower and were less confident walking in comparison to people without spasticity. Specific impairments, however, were not assessed in this study therefore conclusions regarding their influence over the efficacy of FES cannot be made. The relationship between the presence of specific impairments, the effects of FES on these impairments and the impact on gait require further exploration. The group that walked at SSWS of 50.8 m/s were significantly older and had greater disability than the group walking at speeds 40.8 m/s, therefore it is possible that moderating factors such as age and disability could have impacted on the effectiveness of FES. The increase in the O2 cost of walking following FES application in pwMS who walked at SSWS’s 40.8 m/s has not been previously reported. Participants in the faster walking group walked at average speeds of 0.97 ± 0.19 m/s, close to that of healthy controls (1.1–1.3 m/s) [29]. Similar walking speeds in MS have been previously reported in pwMS with mild disability, for
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Figure 1. (a–f) Changes in gait speed (m/s), VO2 and O2 cost with and without FES for pwMS walking at SSWS 5 and 40.8 m/s.
example, Martin et al. [7] (1 m/s) and Burschka et al. [30] (1.17 m/s). Participants in the faster walking group in this study presented with less disability (HAI 2 ± 1.5) and anecdotally reported FES to be more beneficial when walking for longer periods (i.e. 45 min), despite no change being noted in their walking speed. Swain et al. [15] previously reported a varied response to FES with pwMS. Sheffler et al. [31] also noted that other orthotic devices such as ankle foot orthosis produced a variable effect in pwMS, with some patients noting improvements and some noting no change in walking speed. An increase in the O2 cost of walking, as noted in the faster walkers in this study, however, has not been previously reported. It is difficult to be sure of the clinical meaningfulness of the increased O2 uptake especially as this was non-significant (p ¼ 0.084). The minimal detectable change (MDC) reported for VO2 uptake in healthy adults has been previously reported to be between 7 and 10% [21]. There was an increase in oxygen cost of 14% noted in the faster walking group and this appears to be attributable to the effect of FES. However, as the MDC has not been previously reported in MS, it is difficult to say whether this is clinically significant change in this population. In addition, there were significant differences between the two groups with regards to how long participants had used FES and this may have been a confounding factor in the results.
Participants who walked at SSWS 50.8 m/s had used FES for a significantly longer time and may have adjusted to the increased energy demands introduced by FES. In comparison, those walking at SSWS 40.8 m/s had used FES for shorter periods of time and may not have had enough time to adapt. Validation of this theory would require further investigation. Burschka et al. tested the utility of the 6-min walk (6 MW) and the 12-min walk (12 MW) tests and suggested that using tests of longer duration (12 MW) and examining linear decline of walking speed is a more sensitive and informative measure of walking for pwMS particularly those with mild disability [30]. Further investigation to evaluate the impact of FES in people with MS who walk at SSWS40.8 m/s may benefit from using walking tests of longer duration and measuring dynamic features such as linear decline. This could give better insight into the effect of using FES over longer distances where fatigueable foot drop becomes more evident. Motl et al. [32] have demonstrated correlations between walking speed, O2 cost of walking and community ambulation. Walking speed and O2 cost of walking, however, are not the only parameters impacting on community ambulation. Doerksen et al. [33] found that factors such as employment status, environment and perceived self-efficacy may have more of an impact than walking speed on community ambulation for people mildly affected by MS. The pwMS in this study who had SSWS’s
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DOI: 10.3109/17483107.2015.1027296
40.8 m/s may have been influenced more by environmental and personal factors with regards to their continued use of FES. Factors such as increased confidence in walking and a reduction in trips which has been reported previously [14,34] or the ability to change walking speeds which is required for successful community ambulation have been highlighted as important by pwMS [35]. Any future evaluation of the impact of FES on pwMS should consider these factors. There are several limitations which may have contributed to the results, not least the small sample size and the heterogeneity of the population. This small study involved established FES users; therefore, the effects in pwMS who have not previously used FES are not known and need to be examined. Direct measures of impairment were not made; therefore, the contributions of lower limb muscle weakness, muscle fatigue and spasticity in addition to other impairments such as balance deficits, visual loss and cognitive impairment to the effect of FES cannot be determined. This study used limited outcome measures (SSWS and O2 cost of walking); therefore, future studies should evaluate the impact of FES on a range of outcomes including dynamic features of walking such as linear decline, the ability to change walking direction and speed, frequency of trips and falls in addition to the ability to ambulate successfully within the community. Full kinematic gait analysis would also contribute to our understanding of the effect of FES on pwMS walking at different gait speeds and should be included in future research. This is the first study to report the effects of FES in pwMS walking at a range of SSWS and has confirmed previous evidence indicating positive effects of FES in pwMS walking at speeds of 50.8 m/s. The negative impact of FES on the O2 cost of walking in pwMS who walk at speeds40.8 m/s could be an indication that FES may not offer any benefits for this group of pwMS. The results raise questions around the clinical use of FES in this patient group, and further investigation is required to help inform future clinical decisions around the prescription of FES in MS.
Acknowledgements The research team would like to acknowledge the commitment made by all the people with MS who volunteered to participate in this study.
Declarations of interest The authors report no conflict of interest.
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RESEARCH PAPER
The impact of walking speed on the effects of functional electrical stimulation for foot drop in people with multiple sclerosis Disabil Rehabil Assist Technol Downloaded from informahealthcare.com by Fudan University on 05/10/15 For personal use only.
L. Miller1,2, D. Rafferty2, L. Paul3, and P. Mattison1 1
MS Service, NHS Ayrshire and Arran, Scotland, UK, 2School of Health and Life Sciences, Glasgow Caledonian University, Glasgow, Scotland, UK, and School of Medicine, University of Glasgow, Glasgow, Scotland, UK
3
Abstract
Keywords
Purpose: Functional electrical stimulation (FES) is effective in assisting people with multiple sclerosis (pwMS) with gait. Previous studies have investigated the effects of FES in pwMS with slow self-selected walking speeds (SSWS). This study reports on the effect of the Odstock Dropped Foot Stimulator (ODFS) on the speed and oxygen (O2) cost of gait in pwMS walking at a range of SSWS. Methods: Twenty pwMS (mean age 50.4 ± 7.3 years) currently using FES walked at their SSWS for 5 min with and without FES. O2 cost of gait was measured using a gas analysis system, and gait speed was calculated. Data were analysed for all participants, and comparisons were made between those with a SSWS5and40.8 m/s (walking speed required for community ambulation). Results: Significant improvements in the speed and O2 cost of gait were seen using FES in the group with SSWS 50.8 m/s (n ¼ 11, p ¼ 0.005). When participants’ SSWS 40.8 m/s, no difference in gait speed was noted, and a significant increase in O2 cost of gait using FES (n ¼ 9, p ¼ 0.004) was noted. Conclusion: FES has a different effect on the speed and O2 cost of gait dependent on the SSWS of pwMS. This requires further investigation.
Functional electrical stimulation, gait speed, walking History Received 10 August 2014 Revised 23 December 2014 Accepted 5 March 2015 Published online 31 March 2015
ä Implications for Rehabilitation
Functional electrical stimulation (FES) used for foot drop is effective in improving the speed and oxygen cost of walking in pwMS walking at SSWS 50.8 m/s. FES does not seem to have a beneficial effect on the speed and oxygen cost of walking in pwMS walking at SSWS 40.8 m/s. Further research is needed to understand the possible mechanisms involved so that FES for foot drop can be efficiently prescribed.
Introduction In multiple sclerosis (MS), a common neurological condition affecting young adults, walking impairment impacting on disability and participation occurs in around 75% of this population [1–3]. Functional electrical stimulation (FES) is an assistive technology with great potential for restoring movement [4]. When used for foot drop, it is designed to enhance mobility in the home and community. The ability to walk around independently within ones community or ‘‘community ambulation’’ is defined as outdoor walking encompassing activities such as visits to the supermarket, bank or shops, social outings and leisure activities [5]. There is a strong correlation between walking speed and community ambulation in people with multiple sclerosis (pwMS), with selfselected walking speeds (SSWS) of 0.79 m/s being found to be a good indicator of community ambulation [6]. Gait speeds of 0.8 m/s have also been found to be reliable measures of Address for correspondence: L. Miller, School of Health and Life Sciences, Glasgow Caledonian University, Glasgow G40BA, Scotland, UK. E-mail: [email protected]
community ambulation and improved participation in stroke patients [7]. Weakness and fatigue in ankle dorsiflexors contribute to foot drop and impacting on gait in MS. Higher levels of fatigue, increased effort and slower walking speeds have been reported in people with MS, compared to healthy controls [8,9]. FES is used to treat foot drop, and by stimulating the common peroneal nerve via skin surface electrodes the resulting ankle dorsiflexion helps to aid foot clearance. In addition, the stimulation may inhibit antagonists such as the calf muscles and assist flexion at other joints through a flexor withdrawal reflex [10]. FES facilitates a more natural gait pattern, increases circulation and reduces muscle atrophy [11]. There is evidence of an ‘‘orthotic’’ effect of FES on walking in MS and other central nervous system (CNS) disorders [11–19]. An orthotic effect is seen when an individual walks with FES in comparison to walking without FES. Orthotic effects of FES have been noted in pwMS with regards to walking distance and endurance [12], speed and the Physiological Cost Index (PCI) of gait [13–17], oxygen (O2) cost of gait [16,19], falls and occupational performance [17]. Lord et al. [5] suggest that rehabilitation efforts need to be focused to achieve a level of
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mobility sufficient for community ambulation. Previous studies have investigated the effects of FES in pwMS with slow selfselected walking speeds (SSWS) [11,15] and noted significant improvements towards achieving speeds required for community ambulation. There have been no studies reporting the effects of FES in pwMS walking at SSWS 40.8 m/s. There is a need to examine the impact of FES in this group of people with MS in order to determine if there are benefits, so that treatment can be targeted effectively. This paper reports on the effects of the Odstock Foot Drop Stimulator (ODFS), a type of FES device which uses a pressure switch in the heel of the shoe. Previous results from this study which also compared two different types of FES have been previously reported [19]. This study aims to investigate the effect of FES on the speed and O2 cost of gait in pwMS walking at SSWS of 4 and 50.8 m/s.
Materials and methods Ethics Ethics approval was granted from the West of Scotland Research Ethics Committee. NHS Ayrshire and Arran sponsored the study. Subjects The lead clinician identified 56 potential participants with MS from the FES database of NHS Ayrshire and Arran, who met the inclusion/exclusion criteria. They sent the participant information leaflet inviting them to participate in the study. To be included in the study, participants had to: have used ODFS III FES device (OML, Salisbury, UK) for 6 months or more, be able to walk continuously for 5 min and score between 2 (abnormal gait or episodic imbalance; gait disorder is noticed by family and friends; able to walk 25 feet in 10 s or less) and 6 (requires bilateral support and more than 20 s to walk 25 feet; may use wheelchair on occasion) on the Hauser Ambulation Index (HAI) [20]. Potential participants were excluded if they had a recent relapse (within the previous six weeks) or suffered from other neurological disease or co-morbidities restricting gait. Twenty four participants agreed to participate and gave written, informed consent.
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analysis system was fitted to the participants, ensuring the facemask (Hans Rudolph Inc, Kansas City, MO) was comfortable but tight enough to prevent leakage. Gas analysis started 2 min prior to, and continued 2 min after, each walking test. The percentage of expired O2 during over ground gait was used to calculate the O2 cost of gait. This protocol has been previously used by the authors [16,19]. Previous validation of the COSMED system has been undertaken, which found to be acceptable for measuring oxygen uptake in healthy adults over a range of exercise intensities [20]. Test–retest reliability of the oxygen measures for the K4 has been found to be good in healthy adults [21]; however, there has been no previous work in MS. Good to excellent ICC’s have been reported and supports using single point in time measures for this measure [21]. Although there has been no previous validation or reliability of the SSWS in MS, the 6-min walk test has been found to have excellent intra-rater reliability (ICC ¼ 0.950) [22]. Data analysis Descriptive statistics for demographics and baseline variables are presented as means and standard deviations and include; age, time since diagnosis, Hauser Ambulation Index [23], time since using FES. Distance and duration of the walk were recorded. O2 uptake per kilogram body weight (ml/min/kg) and the O2 cost [i.e. physiological cost per unit distance walked (VO2/speed of gait) (ml/min/kg/m)] [24] were recorded and used to analyse the O2 cost of gait during the two conditions. The average of these parameters was calculated using data between minutes 3 and 4 of the walking test when a steady state is achieved [25]. Paired t tests were used to investigate the difference between walking with and without FES with respect to gait speed, O2 uptake and O2 cost of gait. The participants were split into two groups based on their self-selected gait speed (without FES) using the cut off point of 0.8 m/s which defines the walking speed required for community ambulation [9]. A paired t test was used to compare gait speed, O2 uptake and O2 cost of gait with and without FES within each of the groups. The level of significance was set at p50.05, and analysis was performed on Minitab v15 (Coventry, UK).
Procedure The Odstock Dropped Foot Stimulator III (ODFS III) (OML, Salisbury, UK) FES device was used. The ODFS III uses a foot switch placed in the heel of the shoe which detects heel contact and synchronises stimulation of tibialis anterior at heel raise during the swing phase of walking. Before beginning the testing procedure, the ODFS III was checked by a neurophysiotherapist experienced in the application of FES to ensure settings, and electrode position was optimal. A stimulation frequency of 40 Hz was used to stimulate the common peroneal nerve, and the optimal contraction strength was achieved by adjusting the output intensity and the pulse width (3–350 ms). Waveform, ramps and the extension period had been previously optimised to suit each participants gait style and speed. Participants attended on one occasion only and walked on a level floor at their SSWS for 5 min around an elliptical course outlined by two cones 9.5 m apart, giving a 10-m shuttle length. The participants walked once with FES and once without FES with the order of testing being randomised. Participants rested for a minimum of 5 min between tests. A COSMED K4b2 (Cosmed, Rome, Italy) gas analysis system was used to measure the percentage of expired oxygen during over-ground gait. The COSMED system was calibrated prior to each session according to manufacturer’s instructions. Gait speed was calculated by measuring the total distance travelled during each 5 minute walk using a lap counter, tape measure and standard stopwatch. The gas
Results Demographics Of the 24 participants included, four sets of data were excluded from the analysis due to poor fit of face mask resulting in inaccuarte O2 uptake readings(n ¼ 2) and inability of the participant to complete the protocol (n ¼ 2). Table 1 presents the demographics of the remaining participants (n ¼ 20). The mean age was 50.4 ± 7.3 years, time since diagnosis was 11.2 ± 8.6 years, and the HAI score was 4 ± 2.75. The majority of the participants had Relapsing Remitting (RR) MS, and there were equal numbers of males and females. The participants were split into two groups based on their SSWS (without FES), those who walked at SSWS of 50.8 m/s and those who walked at SSWS 40.8 m/s. The group who walked at slower SSWS (50.8 m/s) had significantly greater mean Extended Disability Status Score (EDSS), and Hauser Ambulation Index (HAI) scores were older and had used FES for longer compared to the group who walked at SSWS 40.8 m/s (all p50.01) (Table 1). Orthotic effect of FES on walking speed, O2 uptake and O2 cost of walking Considering all participants (n ¼ 20), pwMS walked significantly faster using FES compared to without (p ¼ 0.043) (Table 2). There were no differences in O2 uptake (p ¼ 0.109) or the O2 cost
Impact of walking speed on FES in MS
DOI: 10.3109/17483107.2015.1027296
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Table 1. Demographics: age, mass, height, body mass index (BMI), time since diagnosis (TSD), Extended Disability Status Scale (EDSS), Hauser Ambulation Index (HAI) and time using FES (tFES) of all participants (n ¼ 20), participants who walked at speeds of50.8 m/s (n ¼ 11) and participants who walked at speeds of 40.8 m/s (n ¼ 9). Group All (n ¼ 20) 50.8 m/s (n ¼ 11) 40.8 m/s (n ¼ 9) p
Age (years)
Mass (kg)
Height (cm)
BMI (kg/m2)
TSD
EDSSa
HAIa
tFESa (years)
50.4 (7.3) 54.2 (7.1) 46.6 (4.5) 40.01
80.4 (20.4) 85.6 (22.5) 74 (16.5) NS
169 (9.5) 170 (8.1) 166 (11.1) NS
28 (5.4) 29.3 (6.3) 26.5 (3.8) NS
11.2 (8.6) 13.1 (8.8) 8.9 (8.2) NS
5.3 (2) 6 (0) 4 (1.5) 40.01
4 (2.75) 5 (2) 2 (1.5) 40.01
2 (5.75) 6 (6) 1 (0.5) 40.01
One-way ANOVA was used to compare groups. Data are reported as means and standard deviations but where data not normally distributed. Values are reported as medians and (IQRs).
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Table 2. Mean walking speed (m/s), O2 uptake (ml/min/kg) and O2 cost (VO2) with and without FES in all participants (n ¼ 20), pwMS who walked 50.8 m/s (n ¼ 11) and pwMS who walked 40.8 m/s (n ¼ 9). Condition
All data (n ¼ 20) Speed (m/s) VO2 (ml/min/kg) Oxygen cost (ml/min/kg/m) pwMS walk 50.8 m/s (n ¼ 11) Speed (m/s) VO2 (ml/min/kg) Oxygen cost (ml/min/kg/m/) pwMS walk 40.8 m/s (n ¼ 9) Speed (m/s) VO2 (ml/min/kg) Oxygen cost (ml/min/kg/m)
NO FES
ODFS
Post-hoc testing
0.69 (0.31) 11.96 (3.0) 0.36 (0.20)
0.73 (0.28) 12.50 (2.71) 0.33 (0.16)
0.043 0.109 0.120
0.46 (0.18) 11.70 (2.40) 0.48 (0.19)
0.53 (0.17) 11.96 (1.35) 0.41 (0.16)
0.005 0.688 0.020
0.97 (0.15) 12.17 (3.76) 0.21 (0.07)
0.97 (0.18) 13.17 (3.77) 0.24 (0.08)
0.744 0.084 0.004
of gait (p ¼ 0.120) when walking with FES in comparison to without FES. The effects of FES on gait in pwMS walking at SSWS 50.8 m/s Participants in the group who walked at SSWS 50.8 m/s had an average gait speed of 0.46 m/s (±0.18) without FES and 0.53 m/s (±0.17) with FES (p ¼ 0.005). There was also a significant reduction in O2 cost of gait with FES in comparison to without (p ¼ 0.02) (Table 2). The effect of FES on gait in pwMS walking at SSWS 40.8 m/s Participants who walked at SSWS 40.8 m/s on average walked at a similar speed with FES (0.97 ± 0.18 m/s) in comparison to without FES (0.97 ± 0.15 m/s) (p ¼ 0.74). There was a nonsignificant increase in O2 uptake (p ¼ 0.84) and a statistically significant increase in O2 cost of walking (p ¼ 0.004) with FES in comparison to without (Table 2). The different effects of FES noted on gait speed, O2 uptake and O2 cost of gait in participants walking at SSWS 40.8 m/s in comparison to those 50.8 m/s are presented in Figure 1 (a–f).
Discussion This study found that walking speed significantly improved with FES compared to without in this cohort of pwMS. FES, however, had a different effect on the speed and O2 cost of gait which was dependent on SSWS. There were significant improvements in the speed and a reduction in O2 cost of gait in those with a SSWS
50.8 m/s, however, those with a SSWS 40.8 m/s demonstrated no improvement in speed and an increase in the O2 cost of gait. This study has confirmed the findings of previous studies in MS [12,16,19] where significant orthotic effects of FES on walking speed have been found. The failure to demonstrate significant improvements in the O2 cost of walking was in contrast to our earlier study using the same protocol [16]. This is the first FES study in MS which has recruited pwMS across a spectrum of disability levels resulting in heterogeneity in the SSWS’s of participants. The participants presented with walking speeds that ranged from 0.21 to 1.23 m/s with a mean walking speed of 0.69 ± 0.31 m/s without FES. Our earlier study [16] evaluated the effect of FES in pwMS who walked at a mean SSWS of 0.43 ± 0.15 m/s, and none of the participants walked at speeds of greater than 0.8 m/s. The current study aimed to recruit participants across a range of disability levels presenting with foot drop which resulted in a number of participants (n ¼ 9) walking at SSWS40.8 m/s. The recruitment of a more heterogeneous sample may have contributed towards a smaller increase in walking speed and the failure to demonstrate a significant reduction in the O2 cost of walking. The greatest benefits from FES in terms of the speed and energy cost of walking were seen in the group who walked at SSWS 50.8 m/s. Weiler et al. [26] had also previously noted that the largest relative gains in walking speed were seen in slower walkers (speeds of 50.3 m/s) in spinal cord injury (SCI) and stroke participants using FES. This, however, has not been previously demonstrated within MS. Barrett et al. [12] suggested that those with MS presenting with lower limb muscle weakness may benefit to a greater extent from the strengthening and reeducation effects of FES than those without muscle weakness. There is also evidence of a positive effect of FES on lower limb spasticity [27] which is more likely to be a symptom for pwMS walking at slower speeds (40.8 m/s). Sosnoff et al. [28] found that pwMS presenting with spasticity in the gastrocnemius and soleus muscles had greater disability, walked slower and were less confident walking in comparison to people without spasticity. Specific impairments, however, were not assessed in this study therefore conclusions regarding their influence over the efficacy of FES cannot be made. The relationship between the presence of specific impairments, the effects of FES on these impairments and the impact on gait require further exploration. The group that walked at SSWS of 50.8 m/s were significantly older and had greater disability than the group walking at speeds 40.8 m/s, therefore it is possible that moderating factors such as age and disability could have impacted on the effectiveness of FES. The increase in the O2 cost of walking following FES application in pwMS who walked at SSWS’s 40.8 m/s has not been previously reported. Participants in the faster walking group walked at average speeds of 0.97 ± 0.19 m/s, close to that of healthy controls (1.1–1.3 m/s) [29]. Similar walking speeds in MS have been previously reported in pwMS with mild disability, for
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Figure 1. (a–f) Changes in gait speed (m/s), VO2 and O2 cost with and without FES for pwMS walking at SSWS 5 and 40.8 m/s.
example, Martin et al. [7] (1 m/s) and Burschka et al. [30] (1.17 m/s). Participants in the faster walking group in this study presented with less disability (HAI 2 ± 1.5) and anecdotally reported FES to be more beneficial when walking for longer periods (i.e. 45 min), despite no change being noted in their walking speed. Swain et al. [15] previously reported a varied response to FES with pwMS. Sheffler et al. [31] also noted that other orthotic devices such as ankle foot orthosis produced a variable effect in pwMS, with some patients noting improvements and some noting no change in walking speed. An increase in the O2 cost of walking, as noted in the faster walkers in this study, however, has not been previously reported. It is difficult to be sure of the clinical meaningfulness of the increased O2 uptake especially as this was non-significant (p ¼ 0.084). The minimal detectable change (MDC) reported for VO2 uptake in healthy adults has been previously reported to be between 7 and 10% [21]. There was an increase in oxygen cost of 14% noted in the faster walking group and this appears to be attributable to the effect of FES. However, as the MDC has not been previously reported in MS, it is difficult to say whether this is clinically significant change in this population. In addition, there were significant differences between the two groups with regards to how long participants had used FES and this may have been a confounding factor in the results.
Participants who walked at SSWS 50.8 m/s had used FES for a significantly longer time and may have adjusted to the increased energy demands introduced by FES. In comparison, those walking at SSWS 40.8 m/s had used FES for shorter periods of time and may not have had enough time to adapt. Validation of this theory would require further investigation. Burschka et al. tested the utility of the 6-min walk (6 MW) and the 12-min walk (12 MW) tests and suggested that using tests of longer duration (12 MW) and examining linear decline of walking speed is a more sensitive and informative measure of walking for pwMS particularly those with mild disability [30]. Further investigation to evaluate the impact of FES in people with MS who walk at SSWS40.8 m/s may benefit from using walking tests of longer duration and measuring dynamic features such as linear decline. This could give better insight into the effect of using FES over longer distances where fatigueable foot drop becomes more evident. Motl et al. [32] have demonstrated correlations between walking speed, O2 cost of walking and community ambulation. Walking speed and O2 cost of walking, however, are not the only parameters impacting on community ambulation. Doerksen et al. [33] found that factors such as employment status, environment and perceived self-efficacy may have more of an impact than walking speed on community ambulation for people mildly affected by MS. The pwMS in this study who had SSWS’s
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DOI: 10.3109/17483107.2015.1027296
40.8 m/s may have been influenced more by environmental and personal factors with regards to their continued use of FES. Factors such as increased confidence in walking and a reduction in trips which has been reported previously [14,34] or the ability to change walking speeds which is required for successful community ambulation have been highlighted as important by pwMS [35]. Any future evaluation of the impact of FES on pwMS should consider these factors. There are several limitations which may have contributed to the results, not least the small sample size and the heterogeneity of the population. This small study involved established FES users; therefore, the effects in pwMS who have not previously used FES are not known and need to be examined. Direct measures of impairment were not made; therefore, the contributions of lower limb muscle weakness, muscle fatigue and spasticity in addition to other impairments such as balance deficits, visual loss and cognitive impairment to the effect of FES cannot be determined. This study used limited outcome measures (SSWS and O2 cost of walking); therefore, future studies should evaluate the impact of FES on a range of outcomes including dynamic features of walking such as linear decline, the ability to change walking direction and speed, frequency of trips and falls in addition to the ability to ambulate successfully within the community. Full kinematic gait analysis would also contribute to our understanding of the effect of FES on pwMS walking at different gait speeds and should be included in future research. This is the first study to report the effects of FES in pwMS walking at a range of SSWS and has confirmed previous evidence indicating positive effects of FES in pwMS walking at speeds of 50.8 m/s. The negative impact of FES on the O2 cost of walking in pwMS who walk at speeds40.8 m/s could be an indication that FES may not offer any benefits for this group of pwMS. The results raise questions around the clinical use of FES in this patient group, and further investigation is required to help inform future clinical decisions around the prescription of FES in MS.
Acknowledgements The research team would like to acknowledge the commitment made by all the people with MS who volunteered to participate in this study.
Declarations of interest The authors report no conflict of interest.
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