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Effects of AFO Use on Walking in Boys With Duchenne Muscular Dystrophy

A Pilot Study

A Pilot Study

Townsend, Elise L. PT, DPT, PhD, PCS; Tamhane, Himani PT, DPT, MS; Gross, K. Douglas PT, DPT, ScD, FAAOMPT, CPed

doi: 10.1097/PEP.0000000000000099
RESEARCH ARTICLE
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Purpose: Although bracing in the late ambulatory stage of Duchenne muscular dystrophy (DMD) has been described, the effects of ankle-foot orthoses (AFOs) in earlier stages have not been evaluated. The aim of this pilot study was to describe the effects of dynamic response AFO (DR-AFO) use in boys with DMD who are ambulatory.

Methods: Using a crossover design, 3 boys were randomly assigned to either a 2-week DR-AFO or a placebo intervention. Phases were separated by a 1-week washout period. Primary outcomes were time to walk 10 m and a 6-Minute Walk Test.

Results: With DR-AFO use, declines in 10-m walk time (median decline = 0.8 s) and 6-Minute Walk Distance (median = 25.0 m) occurred. Parental report suggested that the use of DR-AFOs increased falls in 2 of 3 participants.

Conclusion: This pilot study does not support the use of DR-AFOs by boys with DMD who are ambulatory.

The results of this study do not support the use of dorsal response AFOs (DR-AFOs) in boys with DMD who are ambulatory.

Department of Physical Therapy, School of Health and Rehabilitations Sciences (Drs Townsend and Gross), MGH Institute of Health Professions, Boston, Massachusetts; Massachusetts General Hospital (Dr Townsend), Boston, Massachusetts; Boston University School of Medicine (Dr Gross), Boston, Massachusetts; Health East Medical Center (Dr Tamhane), Englewood, New Jersey.

Correspondence: Elise L. Townsend, PT, DPT, PhD, PCS, Department of Physical Therapy, School of Health and Rehabilitations Sciences, MGH Institute of Health Professions, 36 1st Avenue, Boston, MA 02129. (etownsend@mghihp.edu).

Grant Support: This study was supported by a Marjorie K. Ionta Grant from the MGH Institute of Health Professions awarded to Himani Tamhane.

The authors declare no conflict of interest.

At the time this study was completed, Himani Tamhane was a Master of Science student in the Department of Physical Therapy, School of Health and Rehabilitations Sciences, MGH Institute of Health Professions, Boston, MA, USA.

Duchenne muscular dystrophy (DMD) is an X-linked recessive genetic disorder characterized by progressive muscle weakness that affects functional mobility and participation of boys with DMD, generally by the age of 5 years. Proximal weakness of pelvic, hip, and quadriceps muscles occurs earliest and is more pronounced than distal lower extremity and upper extremity weakness. Gait is typically characterized by widened step width, shorter step length, impaired ankle and hip power, accentuated anterior pelvic tilt with lumbar lordosis, knee recurvatum in stance phase of gait and excessive hip abduction and ankle plantar flexion during swing phase.1 Other common gait compensations for weakness and instability include enhanced lateral trunk lurch, upper extremity abduction, and toe walking.2 Current medical management includes long-term corticosteroids, which may extend ambulation for 1 to 3 years,3–5 particularly if the development of plantar flexion contractures can be avoided. Even with optimal management, slowed, unsteady gait with limited walking endurance is evident by the age of 7 to 9 years, and loss of ambulation by the age of 13 years is expected.6

Orthotics used in the management of DMD include knee-ankle-foot orthoses and ankle-foot orthoses (AFOs). Although knee-ankle-foot orthoses may help prolong walking in the late ambulatory stage for some boys with DMD, their use is associated with reduced walking speed, increased difficulty in stair climbing, and the need for manual assistance to prevent falls.78 Resting AFOs for day or night wear help maintain or slow the loss of ankle plantar flexor muscle length and are an important standard of care for boys with DMD.9 However, solid ankle or hinged AFOs (eg, polypropylene) with a posterior shell are generally not recommended for ambulation in boys with DMD because they fail to provide knee stability and restrict the use of active ankle strategies for balance with standing and walking.10 The added weight of traditional AFOs can further challenge weakened hip muscles and may exacerbate micro-injury of weakened knee extensors during the eccentric loading phase of gait.8

Advances in orthotic design led to development of a lightweight, carbon-composite dynamic response AFO (DR-AFO), which, unlike the traditional solid or hinged AFO, uses an anterior tibial shell thought to assist with knee extension in the mid-stance phase of gait, without preventing inversion and eversion at the ankle. This design aims to reduce proximal joint stresses and assist in overall gait stability. Dynamic response AFOs were designed to use energy stored at heel strike to provide an additional push at toe off and facilitate forward progression.11 Although industry-sponsored research supports the effectiveness of DR-AFOs for ambulation in adults with stroke,12 no studies have examined the effectiveness of DR-AFOs to aid ambulation in children with progressive neuromuscular conditions.

The objective of this pilot study was to assess the feasibility and potential value of future trials and to make a preliminary evaluation of the effects of DR-AFOs on functional mobility and gait in boys with DMD. Our primary aim was to explore how DR-AFO wear affects walking abilities over both household and community distances. A secondary aim was to explore the effects of DR-AFO wear on the challenging functional tasks of stair climbing and rising from the floor, as well as on spatiotemporal gait parameters and fall frequency.

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METHODS

Participants

Three boys with a physician-confirmed diagnosis of DMD were recruited through the Pediatric Neuromuscular Clinic at the Massachusetts General Hospital. Eligible participants were aged 5 to 11 years, had a diagnosis of dystrophinopathy, and were able to ambulate 100 feet or more without resting. Exclusion criteria were the following: (1) attention, language, or cognitive disabilities that limited study participation; (2) ankle plantar flexion contracture(s) greater than 10° that prevented proper orthotic fitting; or (3) ambulation with AFOs at baseline. One participant was excluded for a plantar flexed, supinated ankle/foot with contracture. The study was approved by the hospital's Institutional Review Board. Informed consent of the parent/guardian and assent of the child participants were obtained prior to initiation.

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Study Design

A randomized crossover design was used to compare the effects of a DR-AFO (Figure 1; KiddieGAIT, Allard, USA) to the effects of a placebo neoprene ankle sleeve. The design involved two 2-week intervention phases (1 and 2), separated by a 1-week washout phase, and followed by a 2-week open label period (Figure 2). During phase 1, participants were randomly allocated to use either the DR-AFO (condition sequence A) or the placebo neoprene ankle sleeve (condition sequence B). Both interventions were applied bilaterally. Randomized allocation was conducted using a Web-based random number generator to assign the sequence of conditions. In the washout phase, participants remained intervention free for 1 week. During phase 2, participants used the alternate orthotic. In the open label period, participants wore the preferred orthotic for 2 weeks, which afterward they could keep and continue to use. A total of 5 assessment visits occurred across the 7-week study period. Visits occurred at baseline and at the end of each phase (phase 1, washout, phase 2, and open label). Although complete blinding to intervention condition was not possible, the evaluator was blinded to the sequence of intervention for each child. Participants were told only that the effects of 2 different types of intervention were being explored. Participants wore their usual shoes, which were lightweight, well-fitting sneakers with tie or velcro closure. Orthotics were donated for the purpose of the study and were fitted and adjusted in conjunction with a certified orthotist experienced with DR-AFOs and DMD, based on the published instructions of the manufacturer (http://www.allardint.com/pdf/droppfot/Professional_ToeOFF_Family_AINT.pdf).

Fig. 1

Fig. 1

Fig. 2

Fig. 2

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Outcome Measures

Primary outcome measures were the following: (1) time (s) to walk 10 m and (2) distance (m) covered in a 6-Minute Walk Test, both commonly used as outcome measures in ambulatory DMD trials, and with established reliability, concurrent validity, responsiveness to change, and clinical meaningfulness.6,13–16 The 10-Meter Walk Test was chosen to index short-duration walking speed of household distances. The 6-Minute Walk Distance (6MWD) was chosen to index community walking endurance, with established modifications for boys with DMD that included verbal encouragement during walking to maintain attention to task and a “safety chaser” to walk behind the participant and manage losses of balance and/or falls.16 Secondary outcome measures included (1) timed functional tests of rising to stand from supine and climbing 4 stairs, both reliable and responsive measures of function in boys with DMD that have been used as secondary outcomes in DMD clinical trials6,13,15; (2) spatiotemporal gait parameters including velocity at a self-selected walking speed, step width, and stride length; and (3) fall frequency via parental log. Logs also included days/hours of orthotic use, reports of pain/discomfort with wear, and skin problems.

The order of testing and the durations of rest intervals between tests and procedures were standardized. Timed functional tests were measured in seconds using a digital stopwatch. The better of 2 trials was selected for analysis. Spatiotemporal gait parameters were measured using a 4.9 m GAITRite instrumented walkway system (CIR Systems, Inc, Havertown, PA), which consists of a plastic and rubber mat imbedded with pressure sensors that record footprints. This system has been used with excellent reliability and validity in children with motor disabilities.17 Proprietary GAITRite Software (version 3.9) was used to calculate walking velocity, stride length, and step width, averaged over 4 walking trials. Start and stop lines for each trial were placed 1 m before and after the GAITRite mat so that the initial accelerating and decelerating steps were excluded.

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Data Analysis

Individual difference scores representing change between the start (baseline, no intervention) and the end (with intervention) of each phase were calculated and used to identify median change for each outcome measure. The median was chosen as a measure of central tendency, given the small sample size, high variability of scores, and skewed distributions.18 Inferential statistical tests were not attempted for this small pilot study sample, although descriptive comparisons of median change under the 2 intervention conditions were informative when assessing the potential need for, and feasibility of, future trials.

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RESULTS

Three boys with DMD aged 5 to 11 years participated in this pilot study. All participants were receiving glucocorticoid therapy (for steroid medication and dosing schedule see Table 1) and were independently ambulating in the community, with functional levels ranging from 2 to 3 on the Vignos functional rating scale.19 Change in outcomes with DR-AFO or placebo use are described here and reported in Table 2.

TABLE 1

TABLE 1

TABLE 2

TABLE 2

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Tolerance

All participants were able to attain at least 3 consecutive days of 9 hours daily wear of DR-AFOs. Duration of wear over the 2-week intervention phase ranged from 2 to 11 hours per day (mean = 5.0) for DR-AFOs and 5 to 10 hours per day (mean = 8.0) for the placebo. Individual intervention time means are reported in Table 1. By parent and participant report, negative factors related to DR-AFO wear included more difficulty rising from the floor and climbing stairs and hills and minor skin itching/discomfort. Negative factors related to placebo wear were limited to mild itching and sweating of feet.

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Primary and Secondary Outcomes

Timed Tests. Individual performance data for timed test outcomes are presented in Table 2. With DR-AFO use, median time taken to walk 10 m increased (median increase = 0.8 s [range 0.7-3.4]), whereas median 6MWD decreased (median decrease = −25.0 m [range −44.0 to 18.8]). Median time to rise from the floor was also increased with DR-AFO wear (median increase = 2.7 s [range −0.8 to 4.4]), as was time to climb 4 stairs (median increase = 2.4 s [range 2.2-6.5]). Although these findings are consistent in suggesting worsening walking speed, endurance, rise from the floor time, and stair climb time with DR-AFO use, it is worth noting that high variability in performance was evident for timed tests, both within a single participant across multiple baseline (no intervention) tests and across different participants in terms of the magnitude and/or direction of DR-AFO effects on performance. All 3 boys demonstrated slowed 10-m walk and stair climb times with the DR-AFO intervention, and 2 of 3 showed a decrease in performance in 6MWD and rise from the floor time. However, 1 participant (#3) showed nominally improved performance in 6MWD and rise from the floor time in the setting of high baseline variability. Quantitative evaluation of stability in baseline performance showed that 10-m walk time was the least variable (median baseline difference = 0.3 s [range 0.0-1.0]). Median baseline differences for 6MWD, rise from floor time, and 4 stair climb time were 56.3 m (range 18.8-106.2), 1.7 s (range 0.3-2.2), and 2.8 s (range 0.2-6.4), respectively.

Gait Characteristics. Individual data for gait characteristics are presented in Table 3. Dynamic response AFO wear slowed self-paced median walking velocity in 3 of 3 boys (median = −2.4 cm/s [range −4.5 to 21.7]). Although walking speed was slower with DR-AFO use, both median stride length and median step width were increased (median stride length = 3.5 cm [range −5.8 to 19.9]; median step width = 1.0 cm [range −0.2 to 2.0]), perhaps indicative of a more halting and unbalanced gait with DR-AFO use.

TABLE 3

TABLE 3

Fall Frequency. All participants reported experiencing at least 1 fall during the 1-week washout (no intervention) phase (median = 2 [range 2-4]) and during the 2-week DR-AFO phase (median = 6 [range 1-12]). Consistent with findings of gait characteristics that could suggest a more halting and unbalanced gait pattern during DR-AFO use, 2 of 3 participants also reported a higher frequency of falls during 2 weeks of DR-AFO use, compared with during 2 weeks of placebo use. Individual fall data are summarized in Table 1.

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DISCUSSION

In this pilot study, a small sample of boys with DMD walked more slowly over 10 m, covered less distance in a 6-Minute Walk Test, took longer to rise from the floor and climb stairs, adopted a widened base of support when ambulating, and fell more frequently when wearing DR-AFOs. The slowed speeds when rising from the floor and stair climbing are not surprising. Typical motor patterns for rising from the floor and stair climbing can be impeded by AFO wear that limits talocrural motion near neutral because additional ankle dorsiflexion and plantar flexion are needed to move efficiently with these functional activities. Dynamic response AFOs, which do limit talocrural motion, together with DMD-related muscle weakness, may have conspired to make these functional activities more challenging. Duchenne muscular dystrophy natural history studies confirm that, even without AFOs, rising from the floor and stair climbing become increasingly difficult for boys with DMD, particularly after the age of 7 years.6,15 In this study, the decrease in 4 stair climb speed of all 3 boys exceeded a previously identified minimal clinically important difference (MCID) of 2.1 to 2.2 s,15 suggesting that this loss of speed indeed represented a meaningful decrement in performance.

Performance for primary outcomes of walking speed over 10 m and walking endurance over 6 min also declined with DR-AFO use. Although the slowing of 10-m walk speed did not reach a level of clinical significance (MCID = 1.4-2.3 s), the median decrease in 6MWD was within the MCID range of 20 to 30 m.15 Previous studies have established that the expected changes over time in timed functional test performance (eg, 10-m walk) and 6MWD are strongly influenced by age, baseline ambulatory function, and maturational issues.14,20–22 Although improvements in speed and distance with growth and development may be seen in younger boys, progressive decline is expected after the age of 7 years. In this study, DR-AFO use did not improve 10-m walk speed or 6MWD in a clinically meaningful way in any participant older or younger than 7 years of age.

Findings of a widened base of support and more frequent falls with DR-AFO wear corroborate the prevailing belief that bracing does not improve walking stability in boys with DMD and may even have negative effects on already impaired balance, an idea that has been more theoretically than empirically based.10,23 Given underlying osteopenia and increased risk of femoral and lumbar fractures24 that can bring an end to functional ambulation, fall prevention is an important clinical goal for boys with DMD. More frequent falls with AFO wear implies an increased risk for fall-related fractures, particularly for boys on long-term glucocorticoid therapy.

Mean duration of wear for all 3 participants was higher during the placebo condition than that of DR-AFO condition. Less wear of the DR-AFO could indicate lower tolerance for this intervention, suggesting that the placebo was easier and more comfortable to use. On the contrary, any beneficial effects of treatment using DR-AFOs may not have had the same opportunity to exert themselves because the DR-AFOs were not actually used for the same amount of time as the placebo device. It would be interesting to know, for example, if the reported fall episodes (which were more frequent with DR-AFO use) occurred when the participants were actually wearing the AFOs or during periods when they were not worn. This information was solicited in parental report logs, but was not reported in a clear enough fashion to allow analysis.

The aim of this pilot study was, in part, to assess the feasibility of a future randomized controlled trial of AFO effects on walking in boys with DMD. Given the small sample size of this pilot, statistical comparison of DR-AFO and placebo conditions was not indicated. A comparison of data between the 2 intervention conditions showed high-performance variability, even under baseline (no intervention) conditions, suggesting the need for large sample sizes in any future trials. Potential contributors to day-to-day performance variability include glucocorticoid dosing schedule,25 fatigue,26 and variable motivation/effort.27 Glucocorticoids (eg, prednisone or deflazacort) constitute the only pharmacological therapy with proven potential to decrease (temporarily) the expected decline in motor function in boys with DMD.28,29 Although daily dosing is common, intermittent dosing (eg, 10 days on/10 or 20 days off) has also been studied and recommended, with the aim of achieving similar benefits to muscle and function as with daily dosing, alongside tempered negative side effects including weight gain, stunted growth, bone loss, irritability, and hyperactivity.3,30–32 A statistical comparison of motor performance between corticosteroid “on” and “off” times with intermittent dosing regimens could not be found, but published data suggest that performance on day 10 of corticosteroid dosing is consistently better than at the end of an “off” phase.25 Therefore, intermittent dosing poses an additional challenge to DMD study design and will need to be accounted for in future trials. In addition, future PT intervention studies should consider differences in patterns of change over time between boys younger than 7 years (in whom improvements in timed test performance and 6MWD may occur) and boys 7 years and older (in whom improved performance suggests robust intervention effects)15 and recruit participants accordingly.

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CONCLUSIONS

The findings from this pilot study do not suggest clear benefits with DR-AFO use for household or community ambulation in boys with DMD. Although individual responses vary, DR-AFO wear may slow walking speed over both short and long distances and may be associated with instability and falls for some boys. Additional studies of orthotic use should include a larger sample, collect more detailed fall data, and take into account the potential effect of corticosteroid dosing schedule.

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ACKNOWLEDGMENTS

Dynamic response AFOs were provided by Allard, USA. We thank orthotist Gordon Craig, CO, BOPCO, of New England Orthotic & Prosthetic Systems (NEOPS) for consultation, Brian Tseng, MD, PhD, for an introduction to the study of Duchenne muscular dystrophy and the boys and their families for participation in this study.

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Keywords:

child; Duchenne muscular dystrophy; foot orthoses; gait; male; physical endurance; walking

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