Perceptual & Motor Skills: Physical Development & Measurement 2014, 119, 2, 1-18. © Perceptual & Motor Skills 2014

EFFECTS OF FUNCTIONAL ELECTRICAL STIMULATION ON GAIT RECOVERY POST-NEUROLOGICAL INJURY DURING INPATIENT REHABILITATION1, 2 CHAD I. LAIRAMORE, MARK K. GARRISON, AND LAETITIA BOURGEON University of Central Arkansas MARK MENNEMEIER University of Arkansas for Medical Sciences Summary.—This stage 2 trial investigated the therapeutic effect of single channel, peroneal functional electrical stimulation (FES) for improving gait and muscle activity in people with neurological injuries who were enrolled in an inpatient rehabilitation program. Twenty-six patients (16 male; M age = 51.3 yr., SD = 16.2; 2–33 days post-injury) completed the study. Participants were randomly assigned to an experimental group (n = 13) or control group (n = 13). The experimental group received FES and the control group received sensory stimulation during 45-min. gait training sessions three times a week for the duration of their stay in a rehabilitation facility (average of four sessions for both groups). Changes in gait speed, tibialis anterior muscle electromyography (EMG), and FIM™ locomotion scores were compared between groups. No significant differences were found, as both groups demonstrated similar improvements. The current results with this small sample suggest a low dose of gait training with single channel FES did not augment gait nor EMG activity beyond gait training with sensory stimulation; therefore, clinicians will likely be better served using a larger dose of FES or multichannel FES in this clinical population.

Stroke is the leading cause of disability in the United States with approximately 13 million people having suffered a stroke (Lloyd-Jones, Adams, Carnethon, De Simone, Ferguson, Flegal, et al., 2009). Fifty percent of ischemic stroke survivors over 65 yr. of age exhibit hemiparesis, and thirty percent are unable to walk without assistance (Lloyd-Jones, et al., 2009). In addition, brain injury is a significant contributor to disability in the United States (Faul, Xu, Wald, & Coronado, 2010). Foot drop is a common impairment that leads to disability and limits ambulation in survivors of neurological injury with resulting hemiparesis (Lehmann, Condon, Price, & deLateur, 1987; Lehmann, 1993; DeQuervain, Simon, Leurgans, Pease, & McCallister, 1996; Fish & Kosta, 1999). Single channel functional electrical 1 Address correspondence to Chad Lairamore, University of Central Arkansas, 201 Donaghey Ave., PTC 313, Conway, AR 72035 or e-mail ([email protected]). E-mail addresses for authors are: Mark Garrison ([email protected]), Laetitia Bourgeon ([email protected]), and Mark Mennemeier ([email protected]). 2 This project was supported by NIH Grants DC011824, GM103425, UL1TR000039, and NIGMS IDeA Program Award P30 GM110702.

DOI 10.2466/15.25.PMS.119c19z5

ISSN 0031-5125

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C. I. LAIRAMORE, ET AL.

stimulation (FES) to the peroneal nerve and the tibialis anterior (TA) muscle is an intervention for treating foot drop in patients with hemiparesis. For people with foot drop secondary to chronic stroke (> 6 mo. post), single channel peroneal FES can be effectively used as a neuroprosthesis for its orthotic effect during gait. Numerous studies have demonstrated that when FES is used as a neuroprosthesis it increases gait speed (Burridge, Taylor, Hagan, Wood, & Swain, 1997; Taylor, Burridge, Dunkerley, Wood, Norton, Singleton, et al., 1999; Kottink, Oostendorp, Buurke, Nene, Hermens, & IJzerman, 2004; Robbins, Houghton, Woodbury, & Brown, 2006; Hausdorff & Ring, 2008; Laufer, Hausdorff, & Ring, 2009; Laufer, Ring, Sprecher, & Hausdorff, 2009; Stein, Everaert, Thompson, Chong, Whittaker, Robertson, et al., 2010; Kim, Chung, Kim, & Hwang, 2012). Additionally, use of FES as a neuroprosthesis decreases the physiological demand of walking (Taylor, et al., 1999), improves gait symmetry (Hausdorff & Ring, 2008; van Swigchem, Weerdesteyn, van Duijnhoven, den Boer, Beems, & Geurts, 2011; Kim, et al., 2012), increases balance during gait (Ring, Treger, Gruendlinger, & Hausdorff, 2009), improves obstacle avoidance during gait (van Swigchem, van Duijnhoven, den Boer, Geurts, & Weerdesteyn, 2012), and improves social integration (Laufer, Hausdorff, et al., 2009) for individuals with chronic stroke. In addition to the known orthotic effect of FES, several non-controlled studies have demonstrated prolonged use (3–12 mo.) of single channel peroneal FES may have a therapeutic effect for improving gait in people with chronic stroke. Stein, et al. (2010) found a therapeutic effect on gait performance (4 min. figure eight test) and physiological cost index after using single channel FES for 3 mo. and continued improvements after 11 mo. of use in patients < 6 mo. post-stroke. Laufer, et al. (2009) demonstrated improved gait velocity and single leg stance when patients with chronic stroke walked without FES after using the device for 1 year. Additionally, Everaert, Thompson, Chong, and Stein (2012) revealed use of FES for 3–12 mo. during community ambulation not only increased gait speed for people with chronic stroke, but also increased activation of motor cortical areas as demonstrated by increased motor-evoked potentials from transcranial magnetic stimulation. In contrast to the aforementioned non-controlled studies, a large randomized controlled trial found gait speed was not significantly different when 30 weeks of daily use of FES was compared to 30 weeks of daily use of an ankle foot orthosis (AFO) in people with chronic stroke (Kluding, Dunning, O'Dell, Wu, Ginosian, Feld, et al., 2013). While long-term use of FES may or may not have a therapeutic effect, it is not always feasible as cost and lack of insurance coverage can be prohibitive. Similarly, non-controlled studies investigating the use of single channel peroneal FES for a short duration (≤ 12 weeks) found improved

FES DURING INPATIENT REHABILITATION

3

gait speed and EMG activity in patients with chronic stroke. Hakansson, Kesar, Reisman, Binder-Macleod, and Higginson (2011) found that incorporating FES with fast gait training on a treadmill three times per week for 12 weeks improved gait speed, and Israel, Kotowski, Talbott, Fisher, and Dunning (2011) performed a case series and demonstrated that use of FES for 1 hour three times per week for 6 weeks improved gait speed for one subject. Sabut, Kumar, Lenka, and Mahadevappa (2010) and Sabut, Lenka, Kumar, and Mahadevappa (2010) found that walking with an FES system for 30 min. five times per week for 12 weeks increased gait speed and TA electromyography (EMG) peak amplitude and median frequency. In contrast, randomized controlled trials that have investigated therapeutic effects of short term use (≤ 12 weeks) of single channel peroneal FES for patients with chronic stroke have found that FES assisted gait training is not superior to a control group. Everaert, Stein, Abrams, Dromerick, Francisco, Hafner, et al. (2013) found no significant difference in gait speed nor figure-of-8 walking speed when comparing 12 weeks use of FES for community mobility on a daily basis compared with use of an ankle foot orthosis (AFO) for community mobility in people one year or greater poststroke. Sheffler, Taylor, Gunzler, Buurke, IJzerman, and Chae (2013) found no difference in performance on the lower extremity Fugl-Meyer assessment when comparing the use of FES to normal care with both being provided 2 hours per week for 5 weeks in patients with chronic stroke. Sabut, Sikdar, Mondal, Kumar, and Mahadevappa (2010) suggested incorporating FES into gait training for 30–45 min. 5 days per week for 12 weeks may improve walking ability in patients with chronic stroke; however, they did not find a significant difference in gait speed when comparing the FES and control groups, as both groups improved with therapy. Finally, Pereira, Mehta, McIntyre, Lobo, and Teasell (2012) performed a metanalysis and concluded FES may be effective for improving gait for people with chronic stroke, but it is unclear if FES is superior to other forms of gait training. Only studies which have shown significant improvement from either long-term or short-term use of FES in patients with chronic stroke are those without a control group, while those with control groups indicate there is no improvement attributable to the stimulation—apparently the improvements found in the former studies are due to factors other than the stimulation. In contrast to performing FES during the chronic phase of stroke recovery (> 6 mo. post-stroke), starting FES training earlier, during the subacute stroke recovery phase (< 6 mo. post-stroke), may result in better improvements in walking ability. Studies that have investigated FES during the sub-acute phase of recovery can be divided into two categories: single channel FES and multichannel FES. Multichannel FES consists of stimulating several muscle groups in conjunction with gait or a functional activity

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C. I. LAIRAMORE, ET AL.

as opposed to single channel peroneal FES, which only provides stimulation to the peroneal nerve and TA muscle. Several studies have demonstrated improved gait when multichannel FES is performed in an inpatient rehabilitation setting (Bogataj, Gros, Kljajić, Aćimović, & Malezic, 1995; Yan, Hui-Chan, & Li, 2005; Solopova, Tihonova, Grishin, & Ivanenko, 2011). Yan, et al. (2005) performed 30 min. sessions of multichannel FES to the TA, quadriceps, medial gastrocnemius, and hamstring muscles five times per week for 3 weeks in people with sub-acute stroke and found an increase in TA muscle EMG when compared to a control group. Bogataj, et al. (1995) found that performing multichannel FES to the peroneal nerve and soleus, hamstring, quadriceps, and gluteus medius muscles five times per week for a duration of 30–60 min. for 3 weeks in people with sub-acute stroke resulted in a shorter time to reach independence with gait compared to conventional therapy alone. Solopova, et al. (2011) found that performing multichannel FES to the tibialis anterior, hamstrings, quadriceps, hip adductors, gluteus medius, and gastrocnemius muscles combined with assisted leg movement and progressive limb loading resulted in greater improvements in lower extremity limb function, muscle strength, and muscle activity when compared to a control group. While multichannel FES has been shown to be effective at improving gait for patients with sub-acute stroke, the devices tend to be cumbersome and are not commercially available. In contrast, single channel FES devices are commercially available and less burdensome. Feasibility studies have indicated that single channel FES can be applied during inpatient rehabilitation (Dunning, Black, Harrison, McBride, & Israel, 2009; Salisbury, Shiels, Todd, & Dennis, 2013), while others suggest the use of single channel FES during this time period can improve gait (Sabut, Sikdar, Kumar, & Mahadevappa, 2011; Morone, Fusco, Di Capua, Coiro, & Pratesi, 2012). Sabut, et al. (2011) compared the use of FES-assisted gait training five times per week for 12 weeks in patients with chronic stroke to those with sub-acute stroke and found the sub-acute group demonstrated a 29.4% increase in gait speed as compared to a 17.1% increase in gait speed for the group with chronic stroke. Morone, et al. (2012) found that using single channel peroneal FES for 4 weeks, five times per week for 40 min. during an inpatient rehabilitation program, resulted in increased gait speed when compared against conventional therapy. However, few studies have investigated the efficacy of using single channel peroneal FES during an inpatient rehabilitation program for people with sub-acute stroke. Because of the limited number of studies, several authors have suggested a need for additional randomized controlled trials (Dunning, et al., 2009; Morone, et al., 2012; Salisbury, et al., 2013).

FES DURING INPATIENT REHABILITATION

5

One problem with testing the use of FES in an inpatient rehabilitation facility is the time allotted for inpatient rehabilitation is relatively short (Ottenbacher, Smith, Illig, Linn, Ostir, & Granger, 2004), and a large dose of FES in this setting is not plausible. Therefore, this study was designed as a stage 2 trial (Dobkin, 2009), with treatment parameters that were feasible within real life constraints during rehabilitation. The minimal amount of training and stimulation that might produce significant improvements was evaluated. The purpose of the current research is to assess whether there is a therapeutic effect on gait speed, FIM™ locomotion scores, or TA muscle activity after applying single channel peroneal FES during an inpatient rehabilitation program for patients with sub-acute stroke or brain injury with hemiplegia and resulting foot drop. Hypothesis. Those receiving FES and the control group will both show improvements in gait and muscle activity; greater improvements are expected for the group receiving FES. METHOD Participants Stratified random sampling was used to assign participants to groups and counterbalance the number of participants with stroke and brain injury in each group. Allocation to groups was concealed, performed after signing an informed consent and prior to baseline testing. Participants were informed the study would investigate the effects of a new device on walking but were blinded to group assignment. Thirty-two stroke or brain injury patients were recruited from admissions to an inpatient rehabilitation facility and participated voluntarily. Of the 32 patients recruited, 26 patients (16 male; M age = 51.3 yr., SD = 16.2; 2–33 days post-injury) completed the study. Only those people with nonprogressive forms of brain injury such as traumatic brain injury (n = 3), surgical removal of an aneurysm (n = 1), or stroke (n = 28) were included in the study. Participants were included if they were 18 years old or older, were able to walk 10 meters with moderate or less assistance as determined by the participants’ treating physical therapist using FIM™ guidelines, and had ankle dorsiflexion passive range of motion to 0° or greater. People were excluded if they were receiving other forms of electrical stimulation to the lower extremity, had contra-indications to electrical stimulation, or had any prior condition that limited the ability to walk. Participant characteristics are reported in Table 1.

6

C. I. LAIRAMORE, ET AL. TABLE 1 PARTICIPANT CHARACTERISTICS AND BETWEEN-GROUP COMPARISONS Experimental Group (FES)

Control Group (Sensory)

p

6:7

7:6

.71

15.5 (8.2)

12.9 (5.9)

.45

2–33

6–29

Type of injury (CVA: BI)

11:2

11:2

Sex (male: female)

10:3

6:7

.18

Age (yr.); M (SD)

54.8 (13.4)

47.8 (18.6)

.51

0.43

20–71

22–71

3.9 (1.0)

4.5 (1.2)

.10

0.54

Group Side of hemiplegia (right: left) Days since injury; M (SD) Days since injury; range

Age (yr.); range Number of sessions; M (SD)

ES

0.36

.30

Days enrolled in study; M (SD) 10.4 (3.4) 11.4 (3.9) .49 0.27 Note.—BI, brain injury; CVA, cerebral vascular accident; FES, functional electrical stimulation group. ES = effect size, Cohen's d.

Measures Gait speed.—Gait speed and phases of gait were collected using a GAITRite system3 as participants walked at a comfortable self-selected speed. The test re-test reliability of the GAITRite system for assessing gait parameters for people with stroke enrolled in an inpatient rehabilitation setting is good to excellent, with intraclass correlation coefficients ranging from .72–.94 (Kuys, Brauer, Ada, 2011). The GAITRite walkway contains six arrays of force sensitive sensors imbedded in a walking surface with an active area of 3.66 m long × 0.61 m wide. As participants ambulated across the GAITRite walkway, the system continuously scanned the sensors to detect footfalls and computed temporal and spatial parameters including gait speed and the phases of gait. TA activity in swing and loading.—EMG data during gait were collected from the hemiparetic lower extremity TA muscle at a rate of 2,000 Hz using a Myopac4 16-channel unit. Self-adhesive 2  3 cm silver – silver/chloride passive electrodes5 were used to record surface EMG and serve as the reference electrode. Standardized procedures for EMG electrode placement and data collection were followed based on Surface EMG for NonInvasive Assessment of Muscles (SENIAM) recommendations (Hermens, Freriks, Merletti, Hagg, Stegeman, & Blok, 1999; Hermens, Freriks, Disselhorst-Klug, & Rau, 2000). The reference electrode was placed over the C-7 spinous process. A single researcher performed all electrode placements. CIR Systems, Inc., Havertown, PA RUN Technologies, Mission Viejo, CA 5 Vermed, Bellows Falls, VT 3 4

7

FES DURING INPATIENT REHABILITATION 250 200

loading

stance

swing

150 100 50 0 IC

TO

IC

FIG. 1. Example of enveloped EMG via root mean square (RMS) with phases of gait denoted. IC, initial contact; TO, toe off.

EMG data were synchronized with the GAITRite system so that muscle activity could be examined during the swing and loading phases of gait. The GAITRite system served as the master system for synchronization, outputting a 5 volt signal when data collection was started. This 5 volt signal was detected by the Myopac system triggering simultaneous initiation of EMG data collection, resulting in the data being time synchronized. The data being time synchronized allowed for isolation of EMG data during the swing and loading phases of gait as detected by the GAITRite system. Data processing was performed using a custom analysis program written on MatLab 6.1. EMG data were filtered with a 10–500 Hz band pass filter and enveloped via root mean square (RMS) with 50 msec. intervals. EMG activity was quantified by integration of the RMS signal (RMS area) during the swing and loading phases of gait (Fig. 1). Mean values for each phase of gait were then calculated from the three strides for each participant and normalized to the mean EMG RMS data of the entire gait cycle of the same test, as normalizing to the mean of the gait cycle has been found to decrease variability for the TA muscle. (Yang & Winter, 1984; Winter & Yack, 1987) The change in EMG activity of the tibialis anterior muscle during the swing and loading phases of gait were compared across groups. Locomotion.—FIM™ is a standardized instrument that designates seven major stages in performance on functional activities from completely dependent to independent. In particular, the FIM™ locomotion scores indicates how much assistance is required for a person to walk. The FIM™ instrument has excellent internal consistency for people with neurological disorders (Cronbach's α = .95 Motor-FIM; Hobart, Lamping, Freeman, Langdon, McLellan, & Greenwood, 2001), and meta-analytic findings suggest excellent inter-rater reliability across patients with different diagnosis and levels of impairment (Ottenbacher, Hsu, Granger, & Fiedler, 1996). FIM™ locomotion scores were assigned by the participants' physical therapists at admission to the study and discharge from the hospital, and were derived from the medical records. All physical therapists assign-

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C. I. LAIRAMORE, ET AL.

ing FIM™ locomotion scores were trained in administering the FIM™ and had passed an annual exam administered by the Uniform Data System for Medical Rehabilitation to enhance reliability of scoring. Finally, the amount of change in FIM™ locomotion scores was compared across groups. Procedure The study was approved by a local institutional review board and followed the ethical standards set forth in the Declaration of Helsinki. A 2-group, randomized, parallel-comparison groups design with treatment blinding was implemented. Data were collected prior to interventions and again at the conclusion of the study. The investigator collecting gait speed and EMG data was blinded to treatment groups. Data collection sessions consisted of participants walking 10 meters at a self-selected speed for three repetitions. During data collection, participants walked without the FES device and without any type of ankle orthosis. They were allowed to use a one-handed assistive device during data collection, but were required to use the same device for both pre- and post-testing. In order to minimize the effect of acceleration and deceleration, the GAITRite walkway was placed in the middle of the 10 meters walked and data were collected in the middle 3.66 meters of the distance walked. EMG and spatiotemporal gait parameters were collected simultaneously during the walking task. The primary outcome was the change in gait speed from baseline to post-testing. Secondary analyses were performed on EMG of the TA muscle and FIM™ locomotion scores. All post-testing occurred within a window of 12–48 hr. after the last administration of FES. A Bioness L300™ 6 unit was used to deliver FES (experimental group) or sensory stimulation (control group) during gait training. The Bioness™ L300 is a neuroprosthesis that delivers electrical pulses over the peroneal nerve and the TA muscle, causing the ankle to dorsiflex during the swing phase of gait. The unit was fitted and stimulation parameters set by a single researcher who had previously completed a 2-day course on set up and use of the Bioness™ L300 system. For the experimental group, stimulation was delivered according to the manufacturer's specifications with adequate amplitude to provide ankle dorsiflexion during the swing phase of gait (Bioness, 2006). The intensity of the stimulation varied from 15–76 milliamps (mA), and was set at the lowest amplitude that produced a muscle contraction that provided foot clearance during the swing phase of gait. As mild sensory stimulation is not thought to have an effect on the recovery of gait for people with sub-acute stroke enrolled in a stroke rehabilitation program (Yavuzer, Oken, Atay, & Stam, 2007), sensory stimulation was employed as a control. For the control group, the intensity of stimulation Bioness, Inc., Valencia, CA

6

FES DURING INPATIENT REHABILITATION

9

varied from 3–12 mA and was set at the lowest amplitude that produced a mild sensory stimulus without producing a palpable muscle contraction. Also, to assure there was no motor response in the control group, the Bioness stimulating electrodes were placed over the tibia. For both groups, electrical stimulation was delivered using a continuous, biphasic symmetric waveform with a pulse width of 200 μsec. with a pulse rate of 30 Hz. All participants were enrolled in an inpatient rehabilitation program and received 1.5 hour of physical therapy 5 days per week. During physical therapy sessions, the experimental group received FES and the control group received sensory stimulation over the tibia during gait training three times a week for 45 min. On average participants received FES or sensory stimulation for four sessions over an 11-day time frame. Four physical therapists administered gait training and had a mean of 10 years of experience. The physical therapists were trained to administer gait training (with rest as needed) and no other type of training during the 45-min. sessions. For all participants, gait training was based upon Neuro-Developmental Treatment principles emphasizing the execution of gait with good postural control and normal joint alignment (Howle, 2002). During the gait training sessions, physical therapists provided tactile cues and manual assistance to facilitate a normalized gait pattern. Orthoses or other assistive devices to assist with preventing foot drop were not used during gait training. Instead, moleskin was applied to the anterior plantar surface of participants' shoes to allow the hemiparetic foot to slide forward during gait training. All participants wore the Bioness L300 device during gait training, receiving either sensory stimulation to their tibia or FES, and participants were kept separate during treatment sessions. At the end of data collection, no participants were able to identify if they were in the experimental or control group. Physical therapists performing gait training and assigning FIM™ locomotion scores were aware of the study design, but were not provided group information. However, it is unlikely therapists were truly blinded as they have prior knowledge that FES should elicit a muscle contraction, and the experimental group had a discernible motor response to the FES while the control group did not. Physical therapists were randomly assigned to treat participants in both the experimental and control groups to help minimize any effect of bias. Analysis The change in gait speed, EMG activity of the Tibialis anterior muscle, and FIM™ locomotion scores were compared between groups. Predictive Analytic Software (PASW) Version 17.0 was used for data analysis. Histograms indicated a normal distribution of the data for changes in gait speed and EMG data, and Levene's test for equality of variance was not significant for any of the variables (change in gait speed p = .4, EMG dur-

10

C. I. LAIRAMORE, ET AL.

ing swing / loading p = .81/ p = .35). The data were analyzed for between group differences using independent sample Student’s t tests. Changes in FIM™ locomotion scores, which are ordinal data, were analyzed using a Mann-Whitney test. The largest feasible dose of FES that could be administered during a patient's stay in the rehabilitation facility was small compared to other studies that demonstrated a robust effect size. Morone, et al. (2012) demonstrated that applying FES 5 times per week for 4 weeks for individuals with sub-acute stoke produced a large effect size of 1.13 based on percentage of improvement in gait speed. However, it was only possible to administer FES 3 times per week for 11 days, and therefore a much smaller effect was expected. Because of the small dose and small sample size, statistical testing was lenient to minimize the chance of a type II error; α was set to .05 for all tests. RESULTS Of the 32 participants initially enrolled, 16 were in the experimental group and 16 in the control group (flow of participants is shown in Fig. 2). Three experimental group participants and three control group participants did not complete the study, and their data were excluded. Of these six, one participant withdrew from the study to receive electrical stimulation during cycling. During initial data collection, two participants' stance and swing phases of gait were not possible to determine using the GAITRite system, and both were excluded from the study. Three participants failed to complete the study because they were discharged early from the rehabilitation facility. There was no significant difference between the groups at the onset of the study for gait speed (p = .32, d = 0.17), FIM™ locomotion scores (p = .38, d = 0.09), and EMG activity of the TA muscle during the swing and loading phases of gait (p = .67, d = 0.11; p = .62, d = 0.15). As expected, both groups exhibited improvements in gait from pretest to post-test (Table 2). Within-group comparisons indicated increased gait velocity (FES, p = .005; control, p = .004), increased FIM™ locomotion scores (FES, p = .002; control, p = .002), and increased EMG activity during the swing phase of gait for the FES group (FES, p = .013; control, p = .07). At the conclusion of the study there was no significant difference in the change in gait speed (p = .83), nor change in FIM™ locomotion scores (p = .77) between the experimental and control groups. No significant difference was found in the change in EMG activity of the TA muscle during the swing phase of gait (p = .79), nor in the loading phase of gait (p = .71). Outcomes are presented in Table 2. The mean difference for change in gait speed, the primary outcome measure, had a statistical power of 0.07 and the effect size found for this variable was small (d = 0.17).

FES DURING INPATIENT REHABILITATION

11

Randomized (n=32)

Allocation Allocated to intervention (n=16)

Allocated to intervention (n=16)

(n=15)

(n=15)

Excluded: unable to assess spatiotemporal gait parameters (n=1)

Excluded: unable to assess spatiotemporal gait parameters (n=1)

Follow‐up Lost to follow-up secondary to discharge from the hospital (n=1) Discontinued intervention secondary to participant withdrawal (n=1 )

Lost to follow-up secondary to discharge from the hospital (n= 2)

Analysis Analyzed (n=13)

Analyzed (n=13)

FIG. 2. Experimental design

DISCUSSION This study examined the therapeutic effect of single channel FES used in conjunction with gait training for people with sub-acute stroke or brain injury with hemiparesis and subsequent foot drop who were participating in an inpatient rehabilitation program. While all participants showed improvements from pre-test to post-test, the results indicate that receiving FES did not significantly increase improvements in gait nor TA muscle activity when compared to the control group who received sensory stimulation during gait training. However, it is important to note the small sample size and low statistical power limit the ability to make broad interpretations from this study. In contrast to the current study that used single channel FES to the peroneal nerve and the TA muscle, research that has investigated the therapeutic effect of multichannel FES has found improvements in gait for people with sub-acute stroke (Bogataj, et al., 1995; Yan, et al., 2005; Robbins, et al., 2006; Daly, Zimbelman, Roenigk, McCabe, Rogers, Butler, et al., 2011; Solopova, et al., 2011). Therefore, increasing the number of muscles stimulated with FES may have resulted in different outcomes, and it has been suggested that performing multichannel FES may be more effective than administering single channel FES for people with sub-acute stroke (Robbins, et al., 2006). Therefore, future studies investigating the use of FES with people who have suffered a sub-acute stroke should focus on multichannel FES systems as compared to single channel systems.

1.9

35.9

53.1

0.20

M

1.3

19

20.1

0.14

SD

Control

3.7*

28.7 0.6

8.9

77.5* 23

0.28* 0.21

SD

4.0*

37.2

70.3

0.31*

M

1.5

21.6

33.5

0.21

SD

Control

Post-test Exper. M

Groups

2.2

−2.8

20.2

0.13

M

0.9

25.5

24.9

0.13

SD

Exper.

2.1

1.3

17.2

0.11

M

1.2

29.5

31.2

0.11

SD

Control

Post-test – Pre-test

Difference Within Groups

0.1

−4.1

3

0.02

M Difference

−18.2, 26.4

−25.9, 19.8

−0.11, 0.09

95%CI

FIM locomotion, median score 1 1 4 4 Note.—Exper. = experimental group (n = 13); control group (n = 13). aNormalized to the mean. *Indicates significant change for within-group comparisons from pre-testing to post-testing (p < .05).

0.9

24.6

1.5

31.6

FIM locomotion

EMG TA activity in loadinga

0.09

31.7

0.15

57.3

SD

M

Exper.

EMG TA activity in swinga

Gait speed, m/sec.

Outcome

Pre-test

TABLE 2 MEAN (SD) OF GROUPS, MEAN (SD) DIFFERENCE WITHIN GROUPS, AND MEAN (95%CI) DIFFERENCE BETWEEN GROUPS

12 C. I. LAIRAMORE, ET AL.

FES DURING INPATIENT REHABILITATION

13

Use of FES during inpatient rehabilitation may be beneficial even though this study did not find a difference between the experimental and control groups. Other studies suggest that starting FES early with sufficient intensity may have a long-term benefit for skill acquisition and longterm recovery. Biernaskie, Chernenko, and Corbett (2004) found that a 5 week rehabilitation program (with rodents) started 5 days after infarct produces significantly greater results on a beam traversing task when compared to starting a rehabilitation program 30 days after an infarct and concluded that after a stroke the brain's sensitivity to rehabilitation declines over time. Additionally, employing a crossover design study, Bogotaja, et al. (1995) found that starting FES early was superior to starting the FES protocol later. Additionally, Morone, et al. (2012) found that using single channel peroneal FES for a total of twenty 40 min. sessions over a 4 week duration in patients with sub-acute stroke enrolled in an inpatient rehabilitation program demonstrated a significant increase in gait speed when compared against conventional therapy. Augmentation of gait with single channel FES may therefore depend upon the dosage of treatment. Compared with the study by Morone, et al. (2012), the quantity of FES during the current study was relatively small (M = 3.85 sessions of FES for 45 min. sessions). The low dosage appears to limit the outcome, as a large number of repetitions of movement are required to re-learn a skill and promote neuroplasticy. Kleim and Jones (2008) suggest it is likely that several days of training at a high intensity are required to produce lasting changes in the neural structure. Therefore, future research investigating the use of single channel FES for people with sub-acute stroke should be more robust than the intervention in the current study. As this study was designed as a Stage 2 trial (Dobkin, 2009), the results should not be generalized beyond the setting and dosage, and the results should be confirmed by more rigorous randomized controlled trials. The intent of the study was to examine the effects of FES for gait training while people were participating in inpatient rehabilitation and the dosage was small. The largest feasible dose that could be administered at the facility during the patient's length of stay was provided. The amount of FES received was limited secondary to multiple factors including the physical therapists' schedules; the need to provide training on other functional activities such as bed mobility, transfers, and stair climbing; and the patients' short length of stay once they were able to start walking (M = 11 days), which was not controlled by the research team. This small dosage was likely not sufficient to produce an effect on the participants' gait and muscle activity, and these results should not be interpreted, as FES in general has no therapeutic effect.

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Other limitations include the limited sample and lack of kinematic data. Few patients who were screened at admission to the rehabilitation facility met the inclusion criteria of being able to walk 10 meters with moderate assistance or less. This resulted in a small subset of patients being included in the study. Therefore, one cannot generalize the findings to patients who are non-ambulatory. Additionally, the limited number of partcipants who met the inclusion criteria resulted in a small sample size. Based on the effect size from this study, a sample of 1,142 would be required to achieve a power of 0.8 with a two-tailed α of .05, which is quiet unfeasible in this setting. Finally, this study did not include kinematic data. Kinematic data, particularly measurement of ankle angles in the sagittal plane, may have been more sensitive than EMG for detecting differences in gait between groups. This study indicates that small amounts of FES provided during inpatient rehabilitation (4 sessions for 45 min.) for people with stroke or brain injury may not augment gait nor EMG activity of the TA muscle beyond gait training with sham sensory stimulation. It is likely the low dosage of single channel FES administered during inpatient rehabilitation was not sufficient to induce a therapeutic effect observed in other studies. It is likely that more frequent use of FES for a longer duration or stimulation of multiple muscles is required to achieve improvements in gait and muscle activity. Therefore, further research could build on the results by investigating larger doses and the optimal number of muscles to stimulate during inpatient rehabilitation FES protocols for people with sub-acute stroke. REFERENCES

BIERNASKIE, J., CHERNENKO, G., & CORBETT, D. (2004) Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. Journal of Neuroscience, 24(5), 1245-1254. BIONESS, I. (2006) Ness L300 clinician's guide. Unpublished manuscript, Santa Clarita, CA. BOGATAJ, U., GROS, N., KLJAJIĆ, M., AĆIMOVIĆ, R., & MALEZIC, M. (1995) The rehabilitation of gait in patients with hemiplegia: a comparison between conventional therapy and multichannel functional electrical stimulation therapy. Physical Therapy, 75(6), 490-502. BURRIDGE, J. H., TAYLOR, P. N., HAGAN, S. A., WOOD, D. E., & SWAIN, I. D. (1997) The effects of common peroneal stimulation on the effort and speed of walking: a randomized controlled trial with chronic hemiplegic patients. Clinical Rehabilitation, 11(3), 201-210. DALY, J. J., ZIMBELMAN, J., ROENIGK, K. L., MCCABE, J. P., ROGERS, J. M., BUTLER, K., BURDSALL, R., HOLCOMB, J. P., MARSOLAIS, E. B., & RUFF, R. L. (2011) Recovery of coordinated gait: randomized controlled stroke trial of functional electrical stimulation (FES) versus no FES, with weight-supported treadmill and over-ground training. Neurorehabilitation & Neural Repair, 25(7), 588-596.

FES DURING INPATIENT REHABILITATION

15

DEQUERVAIN, I., SIMON, S., LEURGANS, S., PEASE, W., & MCCALLISTER, D. (1996) Gait pattern in the early recovery period after stroke. Journal of Bone and Joint Surgery, 78, 15061514. DOBKIN, B. H. (2009) Progressive staging of pilot studies to improve phase III trials for motor interventions. Neurorehabilitation & Neural Repair, 23(3), 197-206. DUNNING, K., BLACK, K., HARRISON, A., MCBRIDE, K., & ISRAEL, S. (2009) Neuroprosthesis peroneal functional electrical stimulation in the acute inpatient rehabilitation setting: a case series. Physical Therapy, 89(5), 499-506. EVERAERT, D. G., STEIN, R. B., ABRAMS, G. M., DROMERICK, A. W., FRANCISCO, G. E., HAFNER, B. J., HUSKEY, T. N., MUNIN, M. C., NOLAN, K. J., & KUFTA, C. V. (2013) Effect of a footdrop stimulator and ankle-foot orthosis on walking performance after stroke: a multicenter randomized controlled trial. Neurorehabilitation & Neural Repair, 27(7), 579-591. EVERAERT, D. G., THOMPSON, A. K., CHONG, S. L., & STEIN, R. B. (2012) Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabilitation & Neural Repair, 24(2), 168-177. FAUL, M., XU, L., WALD, M., & CORONADO, V. (2010) Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002-2006. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control. FISH, D., & KOSTA, C. S. (1999) Walking impediments and gait inefficiencies in the CVA patient. JPO, 11, 33-37. HAKANSSON, N. A., KESAR, T., REISMAN, D., BINDER-MACLEOD, S., & HIGGINSON, J. S. (2011) Effects of fast functional electrical stimulation gait training on mechanical recovery in poststroke gait. Artificial Organs, 35(3), 217-220. HAUSDORFF, J. M., & RING, H. (2008) Effects of a new radio frequency-controlled neuroprosthesis on gait symmetry and rhythmicity in patients with chronic hemiparesis. American Journal of Physical Medicine & Rehabilitiation, 87(1), 4-13. HERMENS, H. J., FRERIKS, B., DISSELHORST-KLUG, C., & RAU, G. (2000) Development of recommendations for SEMG sensors and sensor placement procedures. Journal of Electromyography and Kinesiology, 10(5), 361-374. HERMENS, H. J., FRERIKS, B., MERLETTI, R., HAGG, G., STEGEMAN, D., & BLOK, J. (1999) SENIAM 8: European recommendations for surface electromyography. Enschede, Holland: Roessingh Research and Development. HOBART, J. C., LAMPING, D. L., FREEMAN, J. A., LANGDON, D. W., MCLELLAN, D. L., & GREENWOOD, R. J. (2001) Evidence-based measurement: which disability scale for neurologic rehabilitation? Neurology, 57, 639-644. HOWLE, J. M. (2004) Neuro-developmental treatment approach: theoretical foundations and principles of clinical practice. (2nd ed.) Laguna Beach, CA: North American Neurodevelopmental Treatment Association. ISRAEL, S., KOTOWSKI, S., TALBOTT, N., FISHER, K., & DUNNING, K. (2011) The therapeutic effect of outpatient use of a peroneal nerve functional electrical stimulation neuroprosthesis in people with stroke: a case series. Topics in Stroke Rehabilitation, 18(6), 738-745. KIM, J. H., CHUNG, Y., KIM, Y., & HWANG, S. (2012) Functional electrical stimulation applied to gluteus medius and tibialis anterior corresponding gait cycle for stroke. Gait & Posture, 36(1), 65-67.

16

C. I. LAIRAMORE, ET AL.

KLEIM, J. A., & JONES, T. A. (2008) Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. Journal of Speech, Language, and Hearing Research, 51(1), S225-S239. KLUDING, P. M., DUNNING, K., O'DELL, M. W., WU, S. S., GINOSIAN, J., FELD, J., & MCBRIDE, K. (2013) Foot drop stimulation versus ankle foot orthosis after stroke: 30-week outcomes. Stroke, 44(6), 1660-1669. KOTTINK, A. I., OOSTENDORP, L. J., BUURKE, J. H., NENE, A. V., HERMENS, H. J., & IJZERMAN, M. J. (2004) The orthotic effect of functional electrical stimulation on the improvement of walking in stroke patients with a dropped foot: a systematic review. Artificial Organs, 28(6), 577-586. KUYS, S. S., BRAUER, S. G., & ADA, L. (2011) Test-retest reliability of the GAITRite system in people with stroke undergoing rehabilitation. Disability and Rehabilitation, 33(19), 1848-1853. LAUFER, Y., HAUSDORFF, J. M., & RING, H. (2009) Effects of a foot drop neuroprosthesis on functional abilities, social participation, and gait velocity. American Journal of Physical Medicine & Rehabilitation, 88(1), 14-20. LAUFER, Y., RING, H., SPRECHER, E., & HAUSDORFF, J. M. (2009) Gait in individuals with chronic hemiparesis: one-year follow-up of the effects of a neuroprosthesis that ameliorates foot drop. Journal of Neurologic Physical Therapy, 33(2), 104-110. LEHMANN, J. F. (1993) Push-off and propulsion of the body in normal and abnormal gait: correction by ankle-foot orthoses. Clinical Orthopaedics and Related Research, 288, 97-108. LEHMANN, J. F., CONDON, S. M., PRICE, R., & DELATEUR, B. J. (1987) Gait abnormalities in hemiplegia: their correction by ankle-foot orthoses. Archives of Physical Medicine and Rehabilitation, 68(11), 763-771. LLOYD-JONES, D., ADAMS, R., CARNETHON, M., DE SIMONE, G., FERGUSON, T., FLEGAL, K., & HONG, Y. (2009) Heart disease and stroke statistics—2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation, 119, 21-181. MORONE, G., FUSCO, A., DI CAPUA, P., COIRO, P., & PRATESI, L. (2012) Walking training with foot drop stimulator controlled by a tilt sensor to improve walking outcomes: a randomized controlled pilot study in patients with stroke in subacute phase. Stroke Research and Treatment, 523-564. OTTENBACHER, K. J., HSU, Y., GRANGER, C. V., & FIEDLER, R. C. (1996) The reliability of the Functional Independence Measure: a quantitative review. Archives of Physical Medicine and Rehabilitation, 77, 1226-1232. OTTENBACHER, K. J., SMITH, P. M., ILLIG, S. B., LINN, R. T., OSTIR, G. V., & GRANGER, C. V. (2004) Trends in length of stay, living setting, functional outcome, and mortality following medical rehabilitation. JAMA, 292(14), 1687-1695. PEREIRA, S., MEHTA, S., MCINTYRE, A., LOBO, L., & TEASELL, R. W. (2012) Functional electrical stimulation for improving gait in persons with chronic stroke. Topics in Stroke Rehabilitation, 19(6), 491-498. RING, H., TREGER, I., GRUENDLINGER, L., & HAUSDORFF, J. M. (2009) Neuroprosthesis for footdrop compared with an ankle-foot orthosis: effects on postural control during walking. Journal of Stroke & Cerebrovascular Disease, 18(1), 41-47. ROBBINS, S. M., HOUGHTON, P. E., WOODBURY, M. G., & BROWN, J. L. (2006) The therapeutic effect of functional and transcutaneous electric stimulation on improving gait speed in stroke patients: a meta-analysis. Archives of Physical Medicine and Rehabilitation, 87(6), 853-859.

FES DURING INPATIENT REHABILITATION

17

SABUT, S. K., KUMAR, R., LENKA, P. K., & MAHADEVAPPA, M. (2010) Surface EMG analysis of tibialis anterior muscle in walking with FES in stroke subjects. Proceedings of the 32nd Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 5839-5842. SABUT, S. K., LENKA, P. K., KUMAR, R., & MAHADEVAPPA, M. (2010) Effect of functional electrical stimulation on the effort and walking speed, surface electromyography activity, and metabolic responses in stroke subjects. Journal of Electromyography and Kinesiology, 20(6), 1170-1177. SABUT, S. K., SIKDAR, C., KUMAR, R., & MAHADEVAPPA, M. (2011) Improvement of gait and muscle strength with functional electrical stimulation in sub-acute and chronic stroke patients. Proceedings of the 33rd Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2085-2088. SABUT, S. K., SIKDAR, C., MONDAL, R., KUMAR, R., & MAHADEVAPPA, M. (2010) Restoration of gait and motor recovery by functional electrical stimulation therapy in persons with stroke. Disability and Rehabilitation, 32(19), 1594-1603. SALISBURY, L., SHIELS, J., TODD, I., & DENNIS, M. (2013) A feasibility study to investigate the clinical application of functional electrical stimulation (FES), for dropped foot, during the sub-acute phase of stroke – a randomized controlled trial. Physiotherapy Theory and Practice, 29(1), 31-40. SHEFFLER, L. R., TAYLOR, P. N., GUNZLER, D. D., BUURKE, J. H., IJZERMAN, M. J., & CHAE, J. (2013) Randomized controlled trial of surface peroneal nerve stimulation for motor relearning in lower limb hemiparesis. Archives of Physical Medicine and Rehabilitation, 94, 1007-1014. SOLOPOVA, I. A., TIHONOVA, D. Y., GRISHIN, A. A., & IVANENKO, Y. P. (2011) Assisted leg displacements and progressive loading by a tilt table combined with FES promote gait recovery in acute stroke. NeuroRehabilitation, 29(1), 67-77. STEIN, R. B., EVERAERT, D. G., THOMPSON, A. K., CHONG, S. L., WHITTAKER, M., ROBERTSON, J., & KUETHER, G. (2010) Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabilitation & Neural Repair, 24(2), 152-167. TAYLOR, P. N., BURRIDGE, J. H., DUNKERLEY, A. L., WOOD, D. E., NORTON, J. A., SINGLETON, C., & SWAIN, I. D. (1999) Clinical use of the Odstock dropped foot stimulator: its effect on the speed and effort of walking. Archives of Physical Medicine and Rehabilitation, 80(12), 1577-1583. VAN SWIGCHEM, R., VAN DUIJNHOVEN, H. J., DEN BOER, J., GEURTS, A. C., & WEERDESTEYN, V. (2012) Effect of peroneal electrical stimulation versus an ankle-foot orthosis on obstacle avoidance ability in people with stroke-related foot drop. Physical Therapy, 92(3), 398-406. VAN SWIGCHEM, R., WEERDESTEYN, V., VAN DUIJNHOVEN, H. J., DEN BOER, J., BEEMS, T., & GEURTS, A. C. (2011) Near-normal gait pattern with peroneal electrical stimulation as a neuroprosthesis in the chronic phase of stroke: a case report. Archives of Physical Medicine and Rehabilitation, 92(2), 320-324. WINTER, D. A., & YACK, H. J. (1987) EMG profiles during normal human walking: strideto-stride and inter-subject variability. Electroencephalography and Clinical Neurophysiology, 67(5), 402-411. YAN, T., HUI-CHAN, C. W., & LI, L. S. (2005) Functional electrical stimulation improves motor recovery of the lower extremity and walking ability of subjects with first acute stroke: a randomized placebo-controlled trial. Stroke, 36(1), 80-85.

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YANG, J. F., & WINTER, D. A. (1984) Electromyographic amplitude normalization methods: improving their sensitivity as diagnostic tools in gait analysis. Archives of Physical Medicine and Rehabilitation, 65(9), 517-521. YAVUZER, G., OKEN, O., ATAY, M. B., & STAM, H. J. (2007) Effect of sensory-amplitude electric stimulation on motor recovery and gait kinematics after stroke: a randomized controlled study. Archives of Physical Medicine and Rehabilitation, 88(6), 710-714. Accepted July 14, 2014.