Neuroprosthesis for Footdrop Compared with an Ankle-Foot Orthosis: Effects on Postural Control during Walking Haim Ring, MD, MSc,*† Iuly Treger, MD, PhD,*† Leor Gruendlinger, MS,x and Jeffrey M. Hausdorff, PhD‡x//
Objectives: We sought to compare the effects of a radio frequency–controlled neuroprosthesis on gait stability and symmetry to the effects obtained with a standard ankle-foot orthosis (AFO). Methods: A total of 15 patients (mean age: 52.2 6 3.6 years) with prior chronic hemiparesis resulting from stroke or traumatic brain injury (5.9 6 1.5 year) whose walking was impaired by footdrop and regularly used an AFO participated in the study. There was a 4-week adaptation period during which participants increased their daily use of the neuroprosthesis, while using the AFO for the rest of the day. Gait was then assessed in a 6-minute walk while wearing force-sensitive insoles, by using the neuroprosthesis and the AFO in a randomized order. An additional gait assessment was conducted after using the neuroprosthesis for a further 4 weeks. Gait speed and stride time (inverse of cadence) were determined, as were gait asymmetry index and swing time variability. Results: After the 4-week adaptation period, there were no differences between walking with the neuroprosthesis and walking with the AFO (P . .05). After 8 weeks, there was no significant difference in gait speed, whereas stride time improved from 1.48 6 0.21 seconds with the AFO to 1.41 6 0.16 seconds with the neuroprosthesis (P , .02). Swing time variability decreased from 5.3 6 1.6% with the AFO to 4.3 6 1.4% with the neuroprosthesis (P 5 .01). A gait asymmetry index improved by 15%, from 0.20 6 0.09 with the AFO to 0.17 6 0.08 with the neuroprosthesis (P , .05). Conclusions: Compared with AFO, the studied neuroprosthesis appears to enhance balance control during walking and, thus, more effectively manage footdrop. Key Words: Neuroprosthesis—functional electrical stimulation—ankle-foot orthosis—postural control—gait. Ó 2009 by National Stroke Association
Footdrop is one of the common gait impairments associated with hemiplegia; an estimated 20% of all stroke survivors have a footdrop.1 The conventional approach to address footdrop is the prescription of an ankle-foot orthosis (AFO), but this has significant drawbacks.2 Use of an AFO may block normal ankle kinematics during gait and prevent active ankle stability and balance reactions. From the *Neurological Rehabilitation Department, Loewenstein Rehabilitation Center, Ranana, Israel, †Departments of Rehabilitation Medicine, ‡Physical Therapy, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel, xMovement Disorders Unit, Neurology Department, Tel-Aviv Sourasky Medical Center, Tel-Aviv, Israel; and //Division on Aging, Harvard Medical School, Boston, Massachusetts. Received May 19, 2008; revision received August 17, 2008; accepted August 26, 2008. This work was funded in part by Ness Ltd, Ra’anana, Israel.
Sensory feedback that is needed for integrated motor control may also be inhibited with an AFO. Furthermore, it restricts the natural passive range of motion and the flexibility of the ankle and foot, may limit walking ability on uneven terrains, and may be uncomfortable to use.3 AFOs can only be worn in shoes, and often the shoe with the AFO must be larger in size than that of the other foot. Portions of this work were presented at the 15th International World Congress of Physical Therapy in Vancouver, British Columbia, Canada, in June 6, 2007. Address correspondence to Jeffrey M. Hausdorff, PhD, Movement Disorders Unit, Neurology Department, Tel-Aviv Sourasky Medical Center, Weizmann 6 Tel-Aviv, Israel. E-mail: jhausdorff@alum.mit. edu. 1052-3057/$—see front matter Ó 2009 by National Stroke Association doi:10.1016/j.jstrokecerebrovasdis.2008.08.006
Journal of Stroke and Cerebrovascular Diseases, Vol. 18, No. 1 (January-February), 2009: pp 41-47
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As a result, the AFO is often rejected by patients. Geboers et al5 concluded that an AFO does not improve walking performance as measured by a 10-m walk test, and a recent study also showed that, in the long run, the effectiveness of the AFO is minimal.6 Despite these limitations, AFOs have some advantages such as providing firm ankle stability for less cognizant patients. It is also very simple to use and its cost is relatively low. AFOs are probably the most common treatment for footdrop today. Externally induced dorsiflexion using functional electrical stimulation (FES) was initially introduced by Liberson et al7 in 1961 as an alternative treatment for footdrop. Since then, several footdrop stimulators have been developed.3,8-10 Such systems activate the muscles that dorsiflex the ankle and evert the subtalar joint during the swing phase of gait, potentially providing several advantages over the AFO. FES allows both greater passive and active movement of the ankle, promoting proprioceptive input that is essential for postural control.2,11 It does not restrict push-off during the terminal stance, relevant for several patients who have this ability, which is almost totally restricted by the AFO. It enables foot adaptation to uneven terrains, whereas the AFO restricts this adaptation because of its firm structure.12 In addition, there is evidence that stimulation of the common peroneal nerve may trigger knee and hip flexion and thus facilitate the flexion pattern needed for foot clearance during swing.13,14 Other potential benefits of FES are prevention of disuse atrophy, increased local blood flow, and muscle re-education.13,15 These advantages and the ability to program FES parameters to specific patient requirements10 support the idea that FES may be a preferred choice for treating footdrop and might possibly yield better balance control during walking. Despite these potential benefits, clinical use of FES systems for correction of footdrop is not yet common.3 Among the possible reasons for limited use are user-related drawbacks inherent in previously available FES devices15 and the lack of studies documenting improved efficacy of these devices over conventional therapies, such as an AFO. Although several reports have demonstrated the benefits of such systems for the correction of footdrop,3,8,9,16 only two studies directly compared a surface electrode footdrop stimulator with an AFO.17,18 Sheffler et al17 reported promising results, but differences between the two devices did not reach statistical significance and superiority of the FES device over the AFO (or vice versa) could not be definitively established. A recent study by Kottink et al18 evaluated the effects of an implantable peroneal nerve stimulator on walking speed in comparison with the AFO. The participants, stroke survivors with chronic hemiplegia, were randomly allocated to the treatment group or to the control group (who continued their regular use with their AFO). The implanted FES group improved walking speed by 23% whereas the improvement in the control group was only 3%. Although promising, both of
these studies focused on gait speed as their main outcome measure; the effects on other aspects are not known. A new FES neuroprosthesis for the treatment of footdrop (NESS L300, NESS Ltd, Ra’anana, Israel) was recently developed. This system includes features that were intended to overcome barriers in the application of noninvasive FES technology for lower limb activation. The effects of this system on mobility were previously described.19 Consistent with previous FES studies, it was found that gait speed improved and the physiologic costs of walking were also reduced after patients walked with the device for 8 weeks. Here we report on a subgroup of that first study who were tested with the AFO and the neuroprosthesis and compared the conventional treatment for footdrop, the AFO, and the neuroprosthesis, specifically with respect to gait stability and symmetry. These features of gait have been associated with function and fall risk in various populations, even after taking into account gait speed.20-22 Given the system’s ability to adapt in real time,19 we hypothesized that it would enhance gait stability and symmetry, compared with the AFO.
Methods Participants We studied 15 patients with chronic hemiparesis. Participants were recruited from two outpatient clinics in rehabilitation centers. The criteria for patient selection were: (1) diagnosis of an upper motor neuron lesion; (2) chronic phase (.6 months postdiagnosis); (3) footdrop (toe drag during walking); (4) regular use of an AFO as prescribed by a physiatrist; (5) passive ankle range of motion to neutral; (6) ability to walk at least 10 m independently or with a cane; and (7) ability to follow multiple-step directions and score greater than 23 on the Mini Mental State Exam.23 Patients were excluded if they had a cardiac pacemaker, skin lesion at the site of the stimulation electrodes, or major depression as defined by Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition criteria (a potential confounder). Patients were recruited for a larger study designed to evaluate the effects of a neuroprosthesis on gait in patients with footdrop19; the current study is based on a subset of those patients previously described who were tested with their AFO. The criterion for this subset was use of an AFO for at least 6 months before the initiation of the study. Eleven male and 4 female patients participated in the study. Twelve patients were poststroke and 3 patients were posttraumatic brain injury. Six patients had right hemiparesis and 9 had left hemiparesis. The mean age was 52.2 6 3.6 years. The average time postbrain injury was 5.9 6 1.5 years.
The Neuroprosthesis The system includes an electronic orthosis, a control unit, and a gait sensor that communicate by radio signals.
FES VS. AFO FOR FOOTDROP
The orthosis delivers electrical pulses to the common peroneal nerve. These pulses are synchronized by the sensor to activate the ankle dosiflexors during the swing phase of gait and thus prevent footdrop. It may also be configured to stimulate during part of the stance phase to improve ankle stability while weight bearing. The hybrid orthosis, designed to enable accurate and repeatable placement, includes two electrodes (45-mm diameter) and an integrated configurable stimulation unit. The stimulating electrodes are placed by a clinician before use. One electrode is located over the common peroneal nerve, posterior and distal to the fibular head, and a second electrode is located over the tibialis anterior muscle to achieve dorsiflexion with slight eversion. The movement may be further adjusted by modifying the position of the electrodes during the fitting process. The patient can then place the orthosis using one hand. The gait sensor uses dynamic gait recognition algorithms to detect events during walking, and then transmits this information to the rest of the system. It includes a pressure sensor worn underneath the shoe insole at the heel with a small transmitter that is attached to the shoe rim. When the system is turned on, the gait sensor identifies the initiation of the swing phase and triggers the stimulation accordingly. A miniature control unit allows simple operation and displays real-time information regarding the system’s status. A handheld computer personal digital assistant [PDA] with configuration software and interface is used by a clinician to set the parameters of the system (e.g., timing, amplitude, pulse width, pulse frequency) and to adjust it to the patient’s gait characteristics (e.g., whether to add stimulation during the stance time).
The AFO Participants used their own plastic AFOs that were prescribed by a physician during rehabilitation. Six patients used a standard plastic off-the-shelf AFO set in neutral position. Nine patients had a custom AFO with special adjustments: 4 patients had AFOs with a hinge and 5 patients used an AFO with a dorsiflexion assist moment.
Procedures and Intervention Patients provided written informed consent, as approved by our institutional review board. Basic demographic variables were collected as was significant medical history. The stimulation (e.g., intensity, pulse frequency) and gait parameters of the neuroprosthesis (e.g., extended time - the percentage of the stance time that the stimulation continues after heel contact) were configured individually for each patient. There was a 4-week adaptation period during which participants increased their daily use of the neuroprosthesis while using the AFO for the rest of the day. The instructions for the participants were as follows: ‘‘Gradually increase the use of the neuroprosthesis to an hour by the end of the first week, to four
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hours by the end of the second week; you can use the neuroprosthesis up to 6 hours by the end of the fourth week. During the adaptation period, keep using your AFO for at least 2 hours a day.’’ After this 4-week adaptation period, gait was measured under two conditions in a randomized order: (1) while using the neuroprosthesis; and (2) while using the AFO. An additional gait assessment was conducted after 4 more weeks of neuroprosthesis use. During these final 4 weeks, patients were encouraged to use only the neuroprosthesis. During this period of time, the instructions for the participants were as follows: ‘‘Use the neuroprosthesis all day long while walking.’’ Under each condition, patients walked on level ground up and down a 50-m hallway at their self-selected, usual walking speed for 6 minutes while wearing force-sensitive insoles (B&L Footswitches, Tustin, CA) connected to a data logger (JAS Research Inc, Belmont, MA)24 enabling measurement of temporal parameters of gait. The patients were instructed to walk as far as they could in 6 minutes while turning around each time they reached the end of the walkway. Average gait speed was determined by dividing the distance covered in 6 minutes by 360 seconds. Stride time (inverse of cadence) was determined to assess the walking pace. A gait asymmetry index and swing time variability (the single support phase variability of the paretic leg) were calculated as markers of gait stability and fall risk.20,21,25-27 The asymmetry index was determined as follows21,28: 100 3 [(swing paretic – swing nonparetic)/(swing paretic 1 swing nonparetic)]. When the asymmetry index 5 0.0, gait is perfectly symmetric. Symmetry indicates that the swing time is similar in both limbs. Conversely, high asymmetry indicates that weight bearing is unevenly distributed, an imbalance that may lead to an increased risk of falls.21,22,29 The coefficient of variation (CV) of the swing time was determined using previously described methods to quantify balance during walking and the intrinsic dynamics of steady-state walking. The CV is defined by: SD/mean 3 100.20 The CV assesses the variability or dysrhythmicity of gait, a measure previously associated with fall risk.20,27,30 Swing time variability is a measure of dynamic balance that is independent of gait speed.20 To evaluate the participants’ acceptance of the neuroprosthesis, patients were asked to report on their preference regarding the AFO and the neuroprosthesis during the last session of the study (week 8). During the study, the participants were instructed to immediately report any adverse event.
Statistical Analysis A repeated measures analysis of variance, using general linear models, was performed separately for each of the different aspects of gait studied to analyze the effects of the neuroprosthesis use under 3 conditions: AFO, walking with the neuroprosthesis after the adaptation
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period, and walking with the neuroprosthesis after 8 weeks. If there were significant differences among the 3 conditions, post hoc analyses compared the AFO condition with the two neuroprosthesis conditions. Values are summarized as mean 6 SD. A P value less than .05 was considered significant.
Results Gait Measures Table 1 summarizes the group values for each gait parameter under the 3 test conditions and the results for comparisons with the AFO. After the 4-week adaptation period, there were no differences between walking with the neuroprosthesis and walking with the AFO (P . .05). After 8 weeks, the effects of the neuroprosthesis on gait were significantly greater than those seen with the AFO in 3 of the 4 outcomes that were measured. Although there was no significant difference in gait speed with the neuroprosthesis, there was a significant change in stride time, gait asymmetry, and swing time variability. The stride time was shorter (P 5 .02), the gait asymmetry index (Fig 1) was improved (P , .05), and the single limb support of the paretic leg (swing time of the nonparetic leg) also became less variable and more consistent (P , .01).
Patient Perceptions The patients’ perceptions of the neuroprosthesis were very positive. For instance, 13 of the 15 patients reported that they felt more stable with the neuroprosthesis and 14 patients indicated that their gait looked more normal. Compared with the AFO, all 15 patients preferred to use the neuroprosthesis for daily ambulation.
Discussion The purpose of this investigation was to compare the effects of a recently developed FES neuroprosthesis on dynamic postural control with that of a traditional AFO in a group of brain-injured patients long after the time frame when spontaneous changes could possibly be expected. The results support the hypothesis that the use of the studied neuroprosthesis enhances gait symmetry and rhythmicity compared with walking using an
AFO. Previous work suggested that FES can improve certain aspects of gait in chronic hemiparetic patients with footdrop (e.g., an improved energy consumption).3,8,9,16 In this study, we extend those previous findings by demonstrating that the beneficial effects on gait are apparently superior to the benefits achieved with an AFO. During the initial adaptation period, the neuroprosthesis effect on gait was similar to that obtained after chronic use with an AFO, but after 8 weeks, the positive impact of the neuroprosthesis was greater than the AFO. The neuroprosthesis improved the walking rhythmicity, and the gait timing became less variable and more consistent, compared with that seen with the AFO. Although gait speed tended to improve, the changes were not statistically significant. These results suggest that the use of the studied neuroprosthesis is likely to enhance postural control during gait, better than that achieved with an AFO. This study also sheds light on a very important clinical question. In contrast to the common clinical belief that FES has an effect only in the swing phase and, therefore, could not be an alternative for patients who present stability difficulties during the stance phase, a positive effect of the FES during the stance (e.g., more consistent single limb support, enhanced swing symmetry that relies on a more stable stance) was observed. This could be explained by the ability of the neuroprosthesis to extend the stimulation past the heel strike, providing an eccentric contraction of the dorsiflexors during the loading response, which assists the heel-rocker mechanism and gives a better perception of the terrain resulting from direct contact with the shoe. In addition, the foot can be maintained in slight eversion during the initial stance, keeping the movement of the center of pressure through the midline and not along the lateral border, as would often be the case with hemiplegic gait. Further biomechanical studies should confirm these possible explanations. Few studies have evaluated the effects of AFOs on postural stability and balance in hemiplegic patients. Wang et al6 examined the effects of the AFO on balance performance in patients with hemiparesis of short (,6 months) and long (.12 months) duration. The measurements in that study included balance evaluations by the Balance Master and the Berg Balance Scale and gait speed and cadence measurement during a 10-m walk. The authors
Table 1. Effects of AFO and neuroprosthesis on gait Measure
AFO
Neuroprosthesis adaptation
Neuroprosthesis postadaptation
6-min Walk gait speed (m/s) Average stride time (s) Swing time variability, nonparetic leg (%) Swing asymmetry
0.58 6 0.06 1.48 6 0.21 5.3 6 1.6 0.20 6 0.09
0.61 6 0.06 (.953) 1.47 6 0.18 (.971) 5.1 6 2.0 (.436) 0.19 6 0.09 (.406)
0.67 6 0.06 (.142) 1.41 6 0.16 (.022) 4.3 6 1.4 (.009) 0.17 6 0.08 (.048)
Abbreviation: AFO, ankle-foot orthosis. P values in parentheses show results of comparison with AFO (at 4 weeks).
FES VS. AFO FOR FOOTDROP
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Swing Asymmetry (index)
0.24
0.22
0.2
0.18
0.16 AFO
Neuroprosthesis adaptation
Neuroprosthesis post adaptation
Figure 1. Gait asymmetry index in 3 different conditions (AFO, neuroprosthesis adaptation [i.e., after 4 weeks of use], and neuroprosthesis postadaptation [i.e., after 8 weeks]). Error bars reflect SE. Continued use of neuroprosthesis apparently improved interlimb symmetry, above and beyond that seen with AFO.
reported that for patients with hemiparesis for at least 12 months, AFOs did not have a significant impact on balance and gait. Two explanations were proposed for the limited benefits of an AFO, reflecting effects on both the ascending and descending pathways. The proprioceptive input is decreased as a result of ankle supports with restrictive properties, and the physical restrictions on ankle joint movement prevent the re-establishment of a normal ankle strategy.31 Indeed, in the current study, enhanced balance control was achieved while walking with an FES neuroprosthesis, which does not limit ankle movement or decrease proprioceptive input. Another interesting potential explanation may be related to the method of activation. In addition to recruiting the dosiflexors, stimulation of the common peroneal nerve facilitates knee and hip flexion.13,14 The neuroprosthesis used in the current study is based on gait recognition algorithms that are designed to optimize control of the foot movement in the appropriate point of the gait cycle. Rather than simply detecting the gait events (e.g., heel-off and heel contact), the algorithms calculate a moving average of swing/stance time and loading to continuously adapt to various parameters. For instance, when a patient moves from a firm terrain (e.g., hard surfaced floor) to a soft terrain (e.g., lawn, sand), the peak loads will change. The system will immediately react to the changed environment and will adapt accordingly. The precise timing of the foot movement, and the hip and knee flexion facilitation, may allow walking to become more automatic and enable transfer of cognitive resources away from gait. In contrast, this facilitation is less likely to take place while using an AFO. Further investigations using dual task paradigms that have been used to identify the automaticity of gait components27 may be helpful for testing these ideas. Nevertheless, the results did not demonstrate a markedly increased gait speed when using the neuroprosthesis compared with the AFO. The direct action of the neuroprosthesis may improve the safety of gait and patient’s con-
fidence irrespective of the effect on velocity. Furthermore, the patients’ average walking speed with the AFO was 0.6 m/s, which offers little potential for improvement in such a short time and without any special gait training intended to improve gait velocity. These findings are consistent with the findings of Granat et al,9 who also showed an improvement in some gait parameters related to balance but not in gait speed when using a peroneal stimulator. A strength of the current study is the use of the 6-minute walk test. This is a functional test that covers several aspects of gait performance and mobility.32 It differs from the standard 10-m, self-paced test of gait because it requires sustained walking activity over a relatively extended period of time.33 The demonstrated advantages of the FES neuroprosthesis during this functional task highlight the potential relevance of the results to everyday situations. The improvement at 8 weeks also suggests that continued use may lead to further normalization of gait; however, additional studies are needed to evaluate this intriguing possibility. Given a choice between the FES neuroprosthesis and the AFO, all patients preferred the neuroprosthesis for daily ambulation. Several factors may have contributed to this preference for the neuroprosthesis. The effects on gait demonstrated in this study likely played a role, but other potential benefits to the patients such as better appearance, ability to walk with similar-sized shoes, the feeling of more active walking, and lighter weight may have also been involved. The high acceptance rate of the neuroprosthesis, its preference over an AFO, and its positive effect on gait suggest that it may be a preferred choice for use by patients with chronic hemiplegia and may contribute to wider use of this technology in the neurorehabilitation field. However, the specific benefits of this device can be more fully addressed only in a study that compares its effects with other FES systems, perhaps while studying electromyography (EMG) and other biomechanical properties. The readiness of the hemiplegic population and clinicians to routinely use this neuroprosthesis in extended use also remains to be seen. This study has several limitations including the relatively small sample size and the protocol duration (i.e., 8 weeks). Further investigations should be undertaken to confirm the study results with larger populations and longer durations of use. In addition, kinetics and kinematics studies may be useful for more completely characterizing the observed changes. In contrast to the current study, which focused on patients with chronic hemiplegia, it may also be helpful to compare the use of the neuroprosthesis with that obtained with an AFO in patients in the acute and subacute stages of stroke. Another potential limitation of the current study is that the protocol did not include a measurement with the AFO before the adaptation period with the neuroprosthesis. It is possible that the gait
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at 4 weeks with the AFO was affected by the training with the neuroprosthesis during that 4-week period. Although this possibility may have lead to an underestimation of the effects of the neuroprosthesis and cannot be completely ruled out, we suggest that it is not a likely explanation for the observed advantages of the neuroprosthesis. This idea is supported by the fact that the AFO walk was the reference and the fact that all patients had chronic conditions, minimizing the possibility of spontaneous improvement in AFO walking. It is also important to keep in mind that the neuroprosthetic effects may have improved muscle function and timing, even without any device. We used the measurement as a reference at week 4 to reflect the state of the participants who had been using the AFO chronically for many years. Nonetheless, future studies may also wish to compare neuroprosthesis use at 8 weeks with that of AFO and no prosthesis at 8 weeks to more fully understand the observed changes in gait over time.
9.
10.
11.
12.
13.
14.
15.
Conclusions These findings suggest that, compared with an AFO, the studied neuroprosthesis apparently yields better balance control and symmetry during walking and thus may more effectively manage footdrop caused by stroke or traumatic brain injury.
16.
17. Acknowledgments: and participation.
We thank the patients for their time 18.
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47 30. Maki BE. Gait changes in older adults: Predictors of falls or indicators of fear. J Am Geriatr Soc 1997;45:313-320. 31. Bunnell KL, Goldie PA. The difference effects of external ankle support on postural control. J Orthop Sports Phys Ther 1994;20:287-295. 32. Pohl PS, Duncan PW, Perera S, et al. Influence of strokerelated impairments on performance in 6 minute walk test. J Rehabil Res Dev 2002;39:439-444. 33. Eng JJ, Chu KS, Dawson AS, et al. Functional walk tests in individuals with stroke: Relation to perceived exertion and myocardial exertion. Stroke 2002;33:756-761.