PHYS THER
Vol. 89, No. 5, May 2009, pp. 499-506
DOI: 10.2522/ptj.20080241
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Case Reports

Neuroprosthesis Peroneal Functional Electrical Stimulation in the Acute Inpatient Rehabilitation Setting: A Case Series

Kari Dunning, Kristy Black, Andrea Harrison, Keith McBride and Susan Israel

K Dunning, PT, PhD, is Assistant Professor, Department of Rehabilitation Sciences, College of Allied Health Sciences, University of Cincinnati Academic Medical Center, and Director of Clinical Research, Drake Center Rehabilitation, Cincinnati, Ohio. Mailing address: Department of Rehabilitation Sciences, University of Cincinnati, 3202 Eden Ave, Cincinnati, OH 45220-0394 (USA).
K Black, PT, is Physical Therapist, Drake Center Rehabilitation.
A Harrison, PT, was Team Leader for inpatient physical therapy, Drake Center Rehabilitation, at the time this case report was written.
K McBride, PT, is Physical Therapist and Director of Clinical Support and Education, Bioness Inc, Valencia, California, and Assistant Professor, Department of Physical Therapy and Rehabilitation Science, University of Maryland School of Medicine, Baltimore, Maryland.
S Israel, PT, MSPT, is Physical Therapist and a doctoral student, Department of Neuroscience, University of Cincinnati School of Medicine, Cincinnati, Ohio.

Address all correspondence to Dr Dunning at: kari.dunning{at}uc.edu


Submitted August 7, 2008; Accepted January 21, 2009


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Abstract
 
Background and Purpose: Studies have suggested that peroneal nerve functional electrical stimulation (peroneal FES) during walking improves gait in patients with chronic stroke. The effect of peroneal FES during the acute stages of stroke recovery is not known. The purposes of this case report are: (1) to describe differences between walking with and without a neuroprosthesis during the first few weeks after stroke, (2) to offer a clinical perspective on decision making for the use of peroneal FES during acute rehabilitation, and (3) to determine the feasibility of rehabilitation with peroneal FES neuroprostheses during the acute phases of stroke recovery.

Case Description: This case report describes 2 patients with different clinical presentations but both receiving inpatient rehabilitation less than 2 weeks after stroke. Each patient received peroneal FES via a neuroprothesis as tolerated while gait training in therapy.

Outcomes: One patient immediately increased gait speed (128%) and decreased time to perform the Timed "Up & Go" Test (40%) using the neuroprothesis. Both patients immediately increased the 6-Minute Walk Test distance using the neuroprothesis (121% and 101%). The patient who underwent testing with the instrumented walking system also demonstrated improved gait symmetry. After 1 to 3 weeks of using the neuroprothesis, the difference between outcomes with and without the neuroprothesis decreased.

Discussion: It is possible that peroneal FES delivered through a neuroprosthesis during acute stroke recovery may improve gait outcomes. Research is needed to determine proper duration and timing.


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Introduction
 
Studies have suggested that peroneal nerve functional electrical stimulation (peroneal FES) during walking increases gait speed and facilitates normal tibialis anterior muscle electromyographic (EMG) activity among people with stroke.1–5 However, these studies involved people with chronic stroke (>6 months). One reason for this is that previously available peroneal FES systems were not feasible to operate in inpatient settings where clinicians have limited time (eg, due to complicated programming, wires, reliability of reapplying electrodes). New, easy-to-use technologies (neuroprostheses) provide a feasible method of using peroneal FES in the inpatient setting, but the effectiveness of peroneal FES during the acute phase of stroke recovery is not known.

There have been a limited number of studies regarding FES in the inpatient rehabilitation setting after stroke. A recent study by Yan et al6 using multiple surface electrodes an average of 8 days after first stroke among rehabilitation inpatients suggested increased strength (force-generating capacity) and improved walking ability. The multiple surface electrodes were placed on the quadriceps, hamstring, medial gastrocrocnemius, and tibialis anterior muscles of the affected leg.6 This multiple electrode system is not available in most clinics and is not feasible for busy clinicians due to complicated and time-consuming donning and doffing. Additionally, the subjects who received electrical stimulation in the study by Yan and colleagues did not use it in the context of function (ie, walking).

There have been no studies conducted during acute stroke recovery using peroneal FES neuroprotheses that have recently become available. The purposes of this case series report are: (1) to describe differences between walking with and without a neuroprosthesis during the first few weeks after stroke, (2) to offer a clinical perspective on decision making for the use of peroneal FES during inpatient rehabilitation, and (3) to determine the feasibility of rehabilitation with peroneal FES neuroprostheses during the acute phases of stroke recovery.


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Patient History and Review of Systems
 
In recruiting for patients for this case series, our inclusion criteria were: (1) inability to perform enough ankle dorsiflexion to clear the foot during swing-through; (2) first stroke experienced less than 2 weeks prior to intervention; (3) ankle dorsiflexion range of motion (ROM) in the affected lower leg of at least neutral with peroneal FES stimulation; (4) history of independent function prior to stroke, including walking without an assistive device; (5) adequate cognition and communication abilities (≥21/30 on the Modified Mini Mental Status Examination7; (6) age 30 to 70 years; (7) ability to walk 5 m with minimum to moderate assistance (with or without assistive device); and (8) tolerance to peroneal FES stimulation.

Exclusion criteria were: (1) excessive pain in the affected leg (≥5 on a 10-point visual analog scale); (2) participating in any experimental rehabilitation or drug studies; (3) implants such as a cardiac pacemaker or vagal nerve stimulator or implants that generate electrical signals or have moving metal parts; (4) lower motor neuron disease or injury with inadequate response to stimulation; (5) significant swelling in the affected leg extending up to the knee; (6) diseases that would limit wearing of the neuroprosthesis, such as venous stasis, or a history of lower-extremity ulcers, chronic skin conditions, or peripheral neuropathy; (7) pregnancy; and (8) a pre-existing orthopedic condition or history of pain that could limit ambulatory progress (eg, total hip or knee replacement, limited lower-extremity ROM, arthritis).

Using these criteria, inpatient physical therapists briefly described the intervention to eligible patients and asked for verbal permission for the treating therapists to contact them. Both patients described below were chosen for the intervention, and, consequently, this case series report, because they met the inclusion criteria. Prior to participating in the intervention, both patients signed an informed consent statement approved by the local institutional review board.

The first patient was a 50-year-old African American man who was 10 days poststroke. He had a history of cocaine abuse, hypertension, and schizophrenia. His hemorrhagic stroke was located in the left thalamus, extending into the left corona radiata with mass effect in the third ventricle, resulting in right-side hemiplegia.

The second patient was a 66-year-old Caucasian woman who was 9 days poststroke. She had a history of hypertension and peripheral vascular disease. Her hemorrhagic stroke was located in the left brain stem, resulting in right-side hemiplegia.

Clinical Impression

These 2 patients were appropriate for peroneal FES due to their inability to dorsiflex the affected foot during swing-through. In addition, they met the criteria established to ensure safe and successful participation by the patient, effectiveness of the device, and in consideration of contraindications for use of the device.


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Examination
 
At initial testing, patient 1 had right ankle dorsiflexion strength of 4/5 with heel support on the floor and 2/5 without heel support. Other lower-extremity strength was normal except: 4+ for right hip flexion, 3– for right hip extension, 3+ for left hip extension, 4+ for right knee extension, and 4 for right knee flexion. Right ankle dorsiflexion passive range of motion (PROM) was 0 degrees in sitting with knees flexed at 90 degrees. Otherwise, bilateral lower-extremity PROM was normal. At enrollment, the patient was walking during therapy with a single-point cane and minimum assistance, demonstrating consistent foot drop with swing-through. As he was unable to clear his foot during swing-through, the therapist had been wrapping his foot into dorsiflexion with an elastic bandage during gait training.

At initial testing, patient 2 had 0/5 right ankle strength. Otherwise, right lower-extremity strength was: 3 for hip flexion, 2 for hip extension, 2+ for hip abduction, 2 for hip adduction, 1 for knee extension, and 1 for knee flexion. Left lower-extremity strength was normal, and bilateral lower-extremity PROM was normal.

Outcomes measured without and with the L300 neuroprosthesis were the 5-Meter Walk Test (5MWT), the Timed "Up & Go" Test (TUG), and the 6-Minute Walk Test (6MWT). The 5MWT has been recommended as a responsive outcome measure during the first 5 weeks after stroke,8 and gait speed has been shown to be a reliable outcome measure for people undergoing inpatient rehabilitation after stroke.9 The TUG is a timed task in which the patients stood up from a chair, walked 3 m, turned around, and sat down. The amount of time that it takes to perform the TUG has been shown to be a reliable and valid outcome measure for people with stroke.10,11 The 6MWT is a reliable outcome measure for people with stroke that measures the distance walked in 6 minutes.11 Both patients were allowed to rest, as needed, during that 6-minute time.

Additional testing for patient 1 included use of the GAITRite system* to obtain data for gait spatiotemporal parameters, including step length, stride length, and single- and double-leg support time. Patient 2 did not have enough endurance to do GAITRite testing. The coefficient of variation, an output of the GAITRite system that demonstrates gait parameter variation between gait cycles, was used to measure gait cycle consistency. The reliability and validity of data obtained with the GAITRite system have been demonstrated in previous research.12,13 In our facility, the GAITRite is located in the outpatient therapy gym, involving a 5-minute transport by wheelchair from the inpatient unit.

After baseline testing, the patients were fitted for the neuroprosthesis and practiced walking for 5 to 10 minutes prior to testing with the neuroprosthesis. Follow-up outcome testing was repeated weekly. However, due to impaired endurance, patient 2 was unable to finish all 3 tests (5MWT, TUG, and 6MWT) with and without the neuroprosthesis in the same day. Therefore, the 6MWT was performed at baseline, the TUG and 5MWT were performed after 1 week of using the neuroprosthesis, and the tests were alternated thereafter, During follow-up testing, outcomes first were measured without the L300 neuroprosthesis. Outcomes were measured by a licensed and trained physical therapist who was not masked to treatment. For patient 1, all testing was done using a single-point cane and assistance, as needed, for safety (contact guard to minimum assistance for loss of balance). For patient 2, all testing was done using a large-base quad cane and minimum assistance for loss of balance and to advance the affected leg, as needed. Due to ankle instability during stance, patient 2 also wore a Velcro ankle support{dagger} to prevent inversion.

To determine user satisfaction, the patients were asked the following questions at each testing session: (1) "Did the stimulation help walking or make it more difficult?" (2) "Did you like the stimulation during walking?" (3) "If you liked the stimulation, why?" and (4) "If you did not like the stimulation, why?" The therapist also was asked questions regarding the feasibility of using this neuroprosthesis in the inpatient rehabilitation setting.

Clinical Impression

Based on examination data, both patients were determined to be appropriate for peroneal FES during gait training, including neutral ankle dorsiflexion, adequate hip and knee strength, and ability to walk with minimal assistance. We expected that they would demonstrate increased gait speed, normalized gait parameters, decreased TUG time, and increased 6MWT distance when walking with the neuroprosthesis compared with walking without the prosthesis.


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Intervention
 
The Ness L300 neuroprosthesis{ddagger} (Figure) was used daily, Monday through Friday, during gait training. The L300 consists of an in-shoe pressure sensor, a control unit, and an orthotic cuff that holds 2 stimulating surface electrodes (Figure). The 2 surface electrodes are positioned to produce dorsiflexion with slight eversion to provide adequate foot and toe clearance and safe initial contact and loading. One electrode is placed in the origin of the tibialis anterior muscle, and the other electrode is placed over the common peroneal nerve, posterior and proximal to the fibular head. Once the optimal position is established, the orthotic cuff holds the electrodes in place for future treatments, thus increasing the reliability of optimum electrode placement and eliminating the need for daily placement fitting. The pressure sensor, through detecting heel-off and initial contact, activates the system to stimulate ankle dorsiflexion and eversion during the swing phase of gait and terminates stimulation during early stance. This system uses wireless communication. At the initial fitting of the device, frequency, waveform, delays, and ramp up and down times were set to elicit the most-effective contraction during ambulation. A video demonstrating the use of the Ness L300 neuroprosthesis for peroneal functional electrical stimulation during gait training is available.


Figure 1
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  		Figure. Ness L300 neuroprosthesis used for peroneal functional electrical stimulation during gait training.

Therapists were trained in donning and doffing the device. A physical therapist with experience in L300 neuroprosthesis administration performed the initial fitting session and was available for consultation. The duration of daily L300 sessions was dictated by how much the patient walked during therapy.


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Outcome
 
At baseline, patient 1 demonstrated immediate improved outcomes using the L300 neuroprosthesis compared with not using the neuroprosthesis. Gait speed more than doubled (from 13.4 cm/s without the L300 to 42.2 cm/s with the L300), and the 6MWT distance increased 121% (from 13.4 m without the L300 to 30.5 m with the L300) (Tab. 1). Time to perform the TUG decreased 39.5% (from 48.4 seconds without the L300 to 29.3 seconds with the L300) (Tab. 1). Table 2 shows that step length increased for both the left and right legs (158% and 78%, respectively), and the coefficient of variation decreased. Other gait parameters, including increased stride length and percentage of gait cycle spent in single-leg support, also improved.


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  		Table 1. Gait Speed, Timed "Up & Go" Test (TUG), and 6-Minute Walk Test (6MWT) Measurements Without and With the L300 Neuroprosthesis for Patients 1 and 2


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  		Table 2. Gait Parameters for Patient 1 Without and With the L300 Neuroprosthesis

Patient 1 used the L300 neuroprosthesis while walking during therapy, an average of 40 minutes (434 steps) per day for 7 days, with no observable muscle fatigue. Daily duration of L300 stimulation with walking varied from 13 minutes (the first day) to 2 hours 8 minutes. Daily contraction was consistent, and the device and electrodes did not need to be adjusted after the initial fitting.

After 7 days of walking with the L300 neuroprosthesis during therapy, patient 1 demonstrated less foot drop without the device, and the differences between outcomes with and without the device were less dramatic (Tabs. 1 and 2). Thus, it was decided to stop using the neuroprosthesis to further challenge him to actively dorsiflex during swing-through. He was discharged home 25 days poststroke (17 days after starting use of the L300 neuroprosthesis) walking with a single-point cane and no ankle support. The majority of the time his foot cleared during swing-through, but he required standby assistance to walk due to loss of balance.

After the first L300 neuroprosthesis session, patient 1 stated he liked the stimulation because it helped him walk by keeping his foot up instead of dragging. The therapist found the neuroprosthesis easy to use and reported that gait training was easier, requiring her to provide less physical assistance for balance and to advance the patient's right leg.

At baseline (day 1), patient 2 demonstrated a 101% increase in 6MWT distance (from 9.7 m without the L300 to 19.5 m with the L300) (Tab. 1). At 2 and 4 weeks, using the neuroprosthesis still resulted in increased 6MWT distance; however, the differences were less dramatic. As shown in Table 1, after 1 week of using the neuroprosthesis during gait training, gait speed was similar (4%) between walking with and without the device (7.2 and 6.9 cm/s, respectively). After 1 week of using the neuroprosthesis, the patient was able to complete the TUG 14.6% faster with the device than without it (111 and 130 seconds, respectively). By the fourth week, there was little difference in TUG time without and with the neuroprosthesis.

During the first 2 weeks, patient 2 used the L300 neuroprosthesis during gait training an average of 30 minutes (270 steps) per day. Daily duration of L300 stimulation with walking varied from 15 to 42 minutes. After 1 week of using the neuroprosthesis, she began to experience difficulties achieving a dorsiflexion contraction with the device. Although her ankle active dorsiflexion was returning, it fatigued quickly and she demonstrated continued drop foot during gait. Therefore, we felt she could still benefit from peroneal FES and continued to try to use the L300 neuroprosthesis during therapy for 3 more weeks until discharge. Throughout these 3 weeks, the patient demonstrated inconsistent responses using the neuroprosthesis, sometimes showing a good dorsiflexion contraction and other times demonstrating no contraction.

Patient 2 was discharged from inpatient rehabilitation to a skilled nursing unit 5 weeks poststroke (4 weeks after starting use of the L300 neuroprosthesis). At that time, she was walking with a small-base quad cane, an air cast for right ankle support, and contact guard assistance due to loss of balance. She had ankle dorsiflexion strength of 3–, but the movement caused rapid fatigue and still required wrapping with an elastic bandage during gait training.

Prior to trying the L300 neuroprosthesis, patient 2 was afraid of the electrical stimulation, but after the first session walking with the device, she liked it and said it helped her walk. Throughout the next 3 weeks, however, she sometimes said the neuroprosthesis helped and at other times said it did not make a difference. The therapist reported that gait training with the L300 neuroprosthesis was easier, requiring less physical assistance to advance the patient's right leg, but that she was frustrated with the inconsistent contraction after the first week.


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Discussion
 
Central nervous system plasticity and motor learning principles emphasize the importance of task-specific, repetitive practice using close-to-normal movements after stroke.14,15 Research16–20 suggests that earlier intervention may improve outcomes after stroke. Peroneal FES via the L300 neuroprosthesis allowed our 2 patients to experience a more-normal gait 10 days poststroke.

There have been a limited number of studies focusing solely on peroneal FES for people during the acute rehabilitation phase. Yan and colleagues6 tested a 4-channel FES system (not a neuroprosthesis) for inpatients used in a side-lying position within 2 weeks poststroke. By the end of the 3-week treatment, the 13 participants who received FES showed greater increases in EMG ankle dorsiflexion torque and decreases in EMG co-contraction ratios compared with the 15 participants who received placebo FES (P<.05). Although there was never any statistical difference in time to perform the TUG between groups, 76.9% of the FES group was ambulating compared with 50.0% of the placebo group after 3 weeks of training (P<.05).

There have been no studies investigating the effect of peroneal FES via a neuroprosthesis during the acute stages of stroke rehabilitation. A recent study using the L300 neuroprosthesis showed immediate increases in gait speed and symmetry among 24 people with foot drop due to chronic hemplegia.21 After 8 weeks of wearing the neuroprosthesis daily, participants continued to experience increased gait speed (P<.001) and symmetry (P<.001).

For people with chronic stroke, typical neuroprosthetic protocols involve gradually increasing the amount of stimulation weekly to avoid fatigue and minimize adverse skin reaction to electrodes. The patients in this case report used the device as tolerated while walking. For patient 1, duration of walking with L300 neuroprosthesis stimulation varied from 13 minutes to 2 hours 8 minutes, with no evidence of fatigue. For patient 2, duration of walking with L300 neuroprosthesis stimulation varied from 15 to 42 minutes.

After 1 week of using the L300 neuroprosthesis, patient 2 began to experience problems achieving a sufficient contraction for toe clearance. This variability could explain her outcome performance with the neuroprosthesis after the first week. At approximately the same time, she began to demonstrate return of active ankle dorsiflexion. Ankle dorsiflexion PROM remained normal throughout her inpatient stay. In addition, although not formally tested using a standardized spasticity (hypertonicity) tool, the therapist observed no resistance to ankle PROM. Patient 2 also had no observable swelling in the affected lower leg. We tried different electrode placements, different frequencies, and increasing intensity without success in achieving a consistent stimulated contraction during walking. All other factors being negative (eg, no lower-extremity swelling or ankle spasticity or tightness), it may be that patient 2 was having difficulty incorporating her newly acquired active ankle movement with the stimulation during walking.

Another reason for the inconsistent contraction for patient 2 may have been tibialis anterior muscle fatigue. Although the potential mechanisms of fatigue induced by electrical stimulation have been studied,22,23 to our knowledge, the susceptibility of the muscle to fatigue from electrical stimulation during acute stroke recovery is not known. To avoid fatigue, Ness protocols recommend performing 15 minutes of cyclic stimulation (referred to as "training" mode) twice daily during the first week and 20 minutes twice daily during the second and third weeks of using the L300 neuroprosthesis in addition to walking. We did not use cyclic stimulation because our objective was to determine changes with peroneal FES when used during walking. It is possible that patient 2 could have benefited from a controlled dosage progression to avoid fatigue. It is unknown which type of patients would benefit from peroneal cyclic stimulation versus FES with walking versus a combined approach during acute recovery.

There have been no studies to determine optimal timing and duration of stimulation per day during acute recovery after stroke. Animal studies have suggested that early, intense therapy may be harmful, potentially causing delayed increases in cortex lesions due to high glutamate release.20 Preliminary results from the first study of humans to investigate this concept of dosing during acute rehabilitation suggest a higher dose (3 hours) of upper-extremity constraint-induced therapy per day was associated with less motor recovery compared with 2 hours per day.24 This concept is controversial, however, as some animal studies have shown that enriched environments early after injury improved outcomes.20 None of these studies tested electrical stimulation. More studies are needed to determine appropriate dosing of peroneal FES during the acute stages of stroke recovery.

Some authors25 have suggested that neuromuscular stimulation can facilitate motor relearning in hemiplegia, especially in the early phases after stroke. The immediate and dramatic improvement in gait symmetry and speed may have facilitated motor relearning for patient 1. It may be beneficial to introduce peroneal FES as early as possible, considering the most-rapid recovery occurs during the first month after stroke.26,27 However, there have been no studies investigating timing of electrical stimulation after stroke. For example, electrical stimulation early after stroke may be beneficial to facilitate neuromuscular education, maintain or increase strength, and decrease spasticity. If peroneal FES normalizes gait during acute stroke recovery, it may help to decrease impairments that become "habits" in chronic stroke, such as hip circumduction and walking with a stiff leg. Alternatively, it is possible that peroneal FES delivered early after stroke may interfere with motor recovery of the ankle during the gait cycle. Early electrical stimulation following stroke has shown positive outcomes in some upper-extremity studies,28–31 although the majority of these studies utilized cyclic activation, with only one study integrating the stimulation with function.31 More studies are needed to determine appropriate timing and method of delivery of electrical stimulation intervention for the lower limb after acute stroke.

Limitations of this case series should be considered. The outcome tester was not masked to treatment. It is not known whether the patients would have experienced the same improvements if they had not used the L300 neuroprosthesis. Both patients had experienced hemorrhagic stroke. It is possible that people with different types of strokes would respond differently. The physical therapists also suggested that when the patients used the L300 neuroprosthesis for gait training, they demonstrated improved balance, but this was not one of our outcomes tested.

A final limitation is the lack of ankle- specific outcomes that would have been helpful in determining possible mechanisms for improvements (eg, ankle active range of motion [AROM], spasticity, and EMG muscle activity and timing during the gait cycle). To our knowledge, these ankle-specific outcomes have not been shown to be reliable or valid for patients with acute stroke. In our experience with patient 2, ankle dorsiflexion AROM varied by day and her fatigue level.

The purpose of this case series was to determine clinical rehabilitation feasibility. However, future studies are needed for evidence-based practice. Therefore, we will briefly address issues related to research feasibility learned from this case series. Outcome testing procedures need to account for the possibility of limited endurance. Incorporating a masked rater is challenging considering inpatient schedules. In addition, a masked rater would not be familiar with physical and cognitive limitations of the individuals tested, which may present safety concerns. Finally, reliability of ankle-specific measures during the acute phase of recovery after stroke, including strength, AROM, and EMG activity, need to be studied. For example, factors such as time of day, time since last gait training session, and lower-extremity swelling may influence the accuracy of these measures. These factors should be considered in future studies. Future studies also should include randomized controls and longer-term follow-up after discharge.


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Conclusion
 
This case series describes 2 patients with different clinical presentations during acute inpatient rehabilitation. Both patients showed immediate improvement in function and gait with the L300 neuroprosthesis, but their progression of treatment differed. There is limited evidence regarding duration and timing of peroneal FES during acute stroke recovery.


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Footnotes
 
Dr Dunning, Ms Black, Ms Harrison, and Mr McBride provided concept/idea/project design. Dr Dunning and Ms Israel provided writing. Dr Dunning and Ms Black provided data collection. Dr Dunning provided data analysis, project management, fund procurement, institutional liaisons, and clerical support. Dr Dunning, Ms Black, and Ms Harrison provided patients. Dr Dunning and Ms Harrison provided facilities/equipment. Dr Dunning, Ms Black, Mr McBride, and Ms Israel provided consultation (including review of manuscript before submission). Mr McBride is employed by Bioness Inc, the manufacturer of the Ness L300 neuroprosthesis, and had no role in data collection and analysis or project management.

This work was conducted at the Drake Center and was funded by a University of Cincinnati Research Council Grant.

This work was presented at the Combined Sections Meeting of the American Physical Therapy Association; February 6–12, 2009; Las Vegas, Nevada.

* CIR Systems Inc, 60 Garlor Dr, Havertown, PA 19083. Back

{dagger} Velcro USA Inc, PO Box 5218, 406 Brown Ave, Manchester, NH 03103. Back

{ddagger} Bioness Inc, 25103 Rye Canyon Loop, Valencia, CA 91355. Back


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