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Progression of Ankle Plantarflexion Contractures and Functional Decline in Duchenne Muscular Dystrophy

Implications for Physical Therapy Management

Kiefer, Michael, PT, DPT; Bonarrigo, Kelly, PT, DPT; Quatman-Yates, Catherine, PT, DPT, PhD; Fowler, Amanda, PT, DPT, PCS; Horn, Paul S., PhD; Wong, Brenda L., MD

doi: 10.1097/PEP.0000000000000553
RESEARCH REPORTS

Purpose: This study characterizes the progressive loss of ankle dorsiflexion range of motion in boys with Duchenne muscular dystrophy (DMD), the relationship to functional decline, and the implications for physical therapy management.

Methods: Longitudinal data for 332 boys with DMD were extracted from medical records and analyzed. Summary statistics for age, number of visits, ankle dorsiflexion measures, and North Star Ambulatory Assessment (NSAA) scores were computed.

Results: Ankle dorsiflexion motion ranged from −32.5 to 25 degrees. Progression of ankle contractures is demonstrated by a trend line: slope −1.43 per year. NSAA score was estimated to decline approximately 0.23 points per 1 degree of ankle dorsiflexion lost.

Conclusions: The results of this study describe the progression of ankle contractures and functional decline in DMD. The findings may help inform decisions regarding interventions to support participants with DMD and their families.

This study characterizes the progressive loss of ankle dorsiflexion range of motion in boys with Duchenne muscular dystrophy, the relationship to functional decline, and the implications for physical therapy management.

Department of Pediatrics (Drs Kiefer and Wong), University of Massachusetts Medical School, Worcester, Massachusetts; Division of Occupational Therapy and Physical Therapy (Drs Kiefer, Bonarrigo, Quatman-Yates, and Fowler) and Division of Neurology (Drs Kiefer, Bonarrigo, Fowler, Horn, and Wong), Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio; Department of Pediatrics (Dr Horn), University of Cincinnati College of Medicine, Cincinnati, Ohio; Department of Physical Therapy (Dr Quatman-Yates), The Ohio State University, Columbus, Ohio.

Correspondence: Michael Kiefer, PT, DPT, University of Massachusetts Medical School, Department of Pediatrics, 55 North Lake Avenue, Worcester, MA 01655 (Michael.Kiefer@umassmed.edu).

The authors declare no conflicts of interest.

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INTRODUCTION

Duchenne muscular dystrophy (DMD) is an x-linked neuromuscular disorder characterized by progressive muscle degeneration that leads to extreme generalized weakness, contractures, and loss of functional mobility.1 , 2 The onset of symptoms typically begins between 3 and 5 years of age and often presents in the form of motor delays, an inability to jump or run, atypical gait, calf pseudohypertrophy, and proximal muscle weakness.1–3 As the disease progresses, individuals with DMD require increased assistance with mobility and typically lose independent ambulation by early teen years, resulting in dependence on wheelchair for mobility.1 , 4

Physical therapists (PTs) serve a critical role in the care for individuals with DMD in the following capacities: (1) monitoring changes in strength, range of motion, and functional mobility, (2) providing interventions and education for individuals and their families about stretching, positioning, and activity pacing/modification, (3) helping determine equipment and device needs, and (4) identifying supplemental interventions such as serial casting or surgical contracture management. Clinicians can help ease transitions during functional decline by communicating with individuals and their families about what is likely to happen before their next visit, plan for additional interventions, and obtain appropriate equipment.

Improved medical intervention and rehabilitation management for individuals with DMD has contributed to prolonged function and participation in all areas of life. Updated care guidelines recommend an increased focus on anticipatory care including comprehensive multidisciplinary assessments at least every 6 months to address domains of International Classification of Functioning, Disability and Health model, as they relate to the progression of contractures, deformity, loss of function, compromised skin integrity, and pain.5 , 6 Providers in multidisciplinary clinics need to work closely with local health care providers to assess and anticipate disease progression and interventions critical to the preservation of range of motion and function. Studies that aid in the understanding of contracture progression and functional decline can be valuable for supporting the best possible care for individuals with DMD and their families.

Ankle dorsiflexion range of motion is often a focus of PT interventions, as it is one of the first body regions to demonstrate contracture, directly impacts gait and functional mobility, and can lead to pain and skin breakdown.5 , 7 A variety of interventions are available to mitigate declines in ankle dorsiflexion range of motion including stretching, orthotics, serial casting, and surgical intervention.3 , 8 , 9 Although ankle plantarflexion contractures and declines in mobility are expected for individuals with DMD, general patterns in contracture progression and the extent to which loss of dorsiflexion corresponds with decline in functional mobility are unclear. There is currently little evidence to help guide PTs with regard to anticipating contracture progression and planning appropriate interventions prior to the next follow-up visit. The purposes of this study were to characterize the progression of loss of ankle dorsiflexion range of motion, describe the relationship between ankle dorsiflexion range of motion and functional mobility decline, and discuss the implications for PT intervention and management.

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METHODS

Prior to the start of the study, approval was obtained by the Center's Institutional Review Board at Cincinnati Children's Hospital Medical Center. Data were extracted from a medical record registry for individuals with DMD who received physical therapy services at the center between May 26, 2009, and June 6, 2016. Inclusion criteria were as follows: (1) male with a diagnosis of DMD, (2) completed at least 2 visits within 14 months for continuity of care, (3) ankle range-of-motion measurements documented in their medical record. Participants were excluded if they had surgical intervention for contracture management or documentation from the evaluating therapist indicated that the values were unreliable for any reason such as a behavioral concern, pain, or recent injury.

All medical records that met the inclusion and exclusion criteria were carried forward for analysis. Specific data extracted from the registry included date of birth, date of all physical therapy visits, clinical assessment scores for the North Star Ambulatory Assessment (NSAA), and ankle dorsiflexion range of motion. The assessment data were expected to be of high fidelity because all of the reported assessments were completed by licensed PTs who were trained to follow a specific protocol and completed a neuromuscular clinical competency for administration and documentation of the assessments. A participant's walking was determined based on the ability to walk 10 m without support from a caregiver or device. Once a participant could not walk, data from that visit and onward for the participant were excluded from analysis.

Ankle dorsiflexion range of motion was measured with the participant in the supine position with the knees in full available extension. The stationary arm of the goniometer was aligned horizontally along the axis of the tibia and the moving arm of the goniometer aligned approximately 1 inch below the lateral malleolus along the axis of the fifth metatarsal. While maintaining subtalar neutral position as possible, the ankle was stretched into dorsiflexion and the measurement was recorded. The PT recorded range of dorsiflexion past plantigrade as +x°'s and range lacking from plantigrade as −x°'s. Both left (L) and right (R) ankles were measured. The average of the left and right measurements was computed and recorded as LR.

The NSAA is a functional scale developed by the Physiotherapy Assessment and Evaluation Group of the North Star Clinical Network for the assessment of individuals who can walk and with DMD. The scale consists of 17 items that assess an individual's functional ability including items from standing, floor and chair transitions, gait, climbing stairs, to jumping and running. Each item is scored on a 3-point scale: 2 representing “normal,” no obvious adaptations of activity, 1 representing modified method but achieves goal independent of physical assist from another, and 0 representing unable to achieve the task independently. The sum of the scores for all items is computed and used to represent a total score. NSAA scores range from 0 if the individual is unable to complete any of the items to 34 if all of the activities are achieved independently and without modifications to impact the score. Instructions on how to administer the examination are available and can be downloaded at the TREAT NMD site (http://www.researchrom.com/masterlist/view/18).10 , 11

Statistical analyses were completed using SAS statistical software version 9.3 for Windows (SAS Institute, Inc, Cary, North Carolina). A linear mixed model with repeated measures was used to create the trend lines in the figures. The model used a spherical power within subject covariance structure. For Figure 1 (age vs NSAA), a breakpoint in the line creating 2 slopes was determined using minimum Akaike criteria. The individual points in figures represent the raw data. For visual purposes, the nested value within subjects is not repeated. Summary statistics for age at each visit, number of visits, ankle dorsiflexion measures, and NSAA scores for each participant were computed. P values less than .05 were considered statistically significant.

Fig. 1

Fig. 1

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RESULTS

A total of 611 medical records were identified as potential candidates for data extraction. After screening the records using the inclusion and exclusion criteria, 322 unique individuals with an aggregate of 1761 eligible unique visit observations were deemed appropriate for the analysis. The number of visits per participant ranged from 2 visits to 11 visits. The distributions for number of observations, dorsiflexion range of motion, and NSAA scores by chronological age are in Table 1.

TABLE 1

TABLE 1

Fig. 2

Fig. 2

An account of NSAA score in relation to age is in Figure 1. The slope is reported with a break in the line at 7 years of age determined by minimum Akaike information criterion. Prior to 7 years of age, the general trend shows improvement as measured by the NSAA slope as 3.09 points per year, SE 0.25, P < .0001. After 7 years of age, the data decline in NSAA slope −1.86 points per year, SE 0.11, P < .0001. Our cohort is consistent with previously publish data on changes in function in boys with DMD as measures by NSAA.12–14

Ankle dorsiflexion declines as ambulatory individuals with DMD get older (Figure 2). Observed average LR ankle dorsiflexion range of motion was between 32.5 and 25 degrees for participants who could walk. Progression of ankle range of motion has a trend line: slope −1.43, standard error (SE) 0.08, and P < .0001.

Figure 3 graphs the relationship between NSAA scores and ankle dorsiflexion range of motion. According to Mazzone et al,12 , 14 participants with an NSAA score of 22 or greater have a reduced risk of losing walking within 2 years. The graph has a low number of observations with NSAA score of greater than or equal to 22 and less than 0 degree of dorsiflexion range of motion.

Fig. 3

Fig. 3

NSAA scores were dependent on average ankle dorsiflexion range of motion. The progression of ankle range of motion in individuals with DMD is graphed with, slope −0.23, SE 0.023, and P < .0001 (Figure 3). The NSAA score declined with an increase in plantarflexion contracture. Summary of data in relation to performance-based cutoff values of NSAA score 22 and dorsiflexion range of motion 0 or more is shown in Table 2 and Figure 3. Gross motor performance as measured by NSAA and 6-minute walk test has improved for individuals with DMD until 7 years of age, which is further supported by analysis of NSAA performance in this cohort (Figure 1).14 , 15 When NSAA data for participants younger than 7 years are removed, the decline is more severe, slope −0.36, SE 0.02, and P <.0001. This shows a trend of decreased performance of 0.36 points on the NSAA for every degree of ankle dorsiflexion lost.

TABLE 2

TABLE 2

The effect of ankle range of motion accounting for participant age produced the following regression model:

NSAA score = 27.1 + 0.26 × LR − 0.68 × Age + 0.05 × LR × Age

In this model, Age = age in decimal years and LR = average of left and right ankle dorsiflexion range of motion. Using this model, a 9-year-old with 10 degrees of ankle dorsiflexion would have a predicted NSAA of 28 (28.1) while that same 9-year-old with 0 degrees ankle dorsiflexion range of motion would have a predicted NSAA of 21 (20.9).

Summary statistics for a subgroup of participants in which loss of walking was confirmed are shown in Table 3. The summary statistics are from the visit prior to confirmed loss of walking, although exact date of loss was not available in the records.

TABLE 3

TABLE 3

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DISCUSSION

The data demonstrated that a decline in the dorsiflexion range of motion for individuals with DMD was correlated with a decline in function as measured by NSAA. The regression model can help PTs understand how plantarflexion contractures progress as well as the correlation with function. The results of the study offer insight and preliminary quantitative parameters for PTs to help anticipate contracture progression and justify implementation of interventions to address this such as orthotics, serial casting, surgical intervention, increased intensity of home stretching program, and initiation of supported standing programs.

Main et al16 review supplemental intervention for contracture management such as serial casting and surgical correction and discuss considerations for choosing appropriate interventions. A reasonable prediction of contracture progression could help ensure individuals receive supplemental interventions at optimal times, allowing them to use these measures before their contracture becomes too great to benefit from these interventions. It also provides additional information to the child's family, as they seek to understand the progression of contractures and the importance of their role in managing contractures as a part of their home program.

Understanding and predicting the effect of contractures on function can provide insight regarding timing of equipment needs. Decline in function and ultimately loss of walking are currently primary drivers for clinical recommendations regarding equipment procurement such as the stander or wheeled mobility device. Understanding the rate of disease progression can improve anticipatory care and timing of equipment and intervention recommendation prior to loss of functional mobility and standing. Literature supports the use of standing devices to positively affect bone mineral density, slow progression of scoliosis, improve lung function, and help maintain lower extremity range of motion.17 , 18 Recommended doses for children with neuromuscular dysfunction is 60 to 90 minutes per day for effects on bone mineral density and 45 to 60 minutes per day for range of motion.17 , 18

A study of tolerability of supported standing in boys with DMD identified ankle plantarflexion contracture as a possible limiting factor in tolerance for duration and position of supported standing.19 Obtaining a stander can take several months, during which time further loss of range of motion, function, and reduced tolerance to supported standing may occur. Understanding the progression of plantarflexion contractures may be useful to inform clinical decision-making regarding timing of device procurement and implementation of supported standing program to improve tolerance and optimize benefits.

Current care guidelines recommend receiving a comprehensive multidisciplinary evaluation and standardized assessment at least every 6 months as well as individualized ongoing physical therapy. Improvements in management of DMD provide an opportunity to prolong mobility and participation, but consistent monitoring of contractures, equipment, and orthotic needs is vital to optimize care and outcomes.

Despite evidence to support the necessity of close monitoring to enhance outcomes, many individuals with DMD are seen at lower-than-recommended frequency both in multidisciplinary clinics and by local PTs. Many factors may influence a child and family's ability to attend recommended care, such as access to services, health literacy, level of acceptance, and financial hardships. The updated care considerations state, “Assessment and anticipatory management must be provided across all domains of the international Classification of Functioning, Disability and Health (ICF), from diagnosis onwards, to minimize contractures, deformity, loss of function, compromised skin integrity, pain, and compromised cardiorespiratory status.”5 , 6 The ability to anticipate needs is critical when considering care for people with a progressive disease especially for those whose health care outcomes may be further complicated by decreased access or adherence to recommendations.

Due to the retrospective nature of the study, the authors could not control for variation in medical or physical therapy intervention. All individuals at this center received standard education at initial evaluation including activity recommendations, risk of loss of range of motion, orthotic use, and importance of home stretching program. Standard recommendations for preservation of range of motion at this center are custom solid ankle foot orthotics set at a comfortable end range worn 8 hours per day (typically overnight), passive ankle stretching once per day for a total of 90 seconds, and positional and self-stretching as the child is able. It is also recommended that the individual see a local PT at least every 3 to 4 months to monitor range of motion and coordinate ongoing needs with primary neuromuscular team. At late walking stage, stander use is recommended; however, initiation is limited depending on equipment availability and participant tolerance. The effect of these recommended interventions has not fully been studied. Prospective analysis controlling for these factors could provide additional information on the efficacy of these interventions on maintaining range of motion and function.

Steroids have become the standard of care for individuals with muscular dystrophy due to the documented effect of glucocorticosteroids on function in people with DMD and potential to prolong ambulation.20–22 Steroid use can vary with regard to the type of steroid, time of initiation, and dosage. Due to the retrospective nature of the study, complete steroid history of each participant was not available. The following steroid regimen guidelines were used at this center to titrate to participants' responses and side effects in line with guideline recommendations: (1) children may be started on intermittent dosing regimen of 10 days on/10 days off to allow for normal height growth while receiving the motor benefits of steroid therapy depending on the severity of motor dysfunction, (2) optimal deflazacort dose is 0.9 mg/kg per day—maximum dose 36 mg per day, (3) optimal prednisone dose is 0.75 mg/kg per day, maximum dose is 30 mg per day.

All measurements were obtained by PTs trained in neuromuscular evaluation; however, with functional testing and range-of-motion measurements, some inter- and intrarater reliability error is expected. With a progressive diagnosis of DMD, a study visit window of 6 to 14 months between appointments provides opportunity for changes in mobility and function during that period. Decline in performance may be accelerated as an individual nears loss of walking. Depending on where the decline falls in the window between visits, some meaningful information may be missed by the care providers. In addition, events such as a fall or fracture can lead to sudden loss of walking prior to when it might otherwise be expected to occur. There is variability in the number of visits per subject due to the nature of the data set. Despite the effect of these limitations, the authors believe that the robust sample size and consistency of measurement provides valuable data from which to discuss the management of ankle contractures in for people with DMD.

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CONCLUSIONS

The results from this study document plantarflexion contracture progression and functional mobility decline for a cohort of people with DMD. Clinicians can use this information to assist in anticipating the progression of plantarflexion contractures and changes in function in people with DMD and make timely decisions regarding intervention and equipment needs. With continued improvements in disease-modifying therapies, clinicians will benefit from information to assist in the understanding of disease progression, as it relates to contractures and functional mobility, to provide more focused anticipatory and preventative care. A multicenter prospective study, controlling for adherence to care recommendations and closer monitoring of participants, could provide further validation of the result in the current study while improving the ability to predict the rate of contracture progression and functional decline.

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Keywords:

ambulatory assessment; contracture; DMD; Duchenne muscular dystrophy; gastrocnemius; muscular dystrophy; North Star heel cord; NSAA; range of motion; ROM

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