Gait and Sit-To-Stand Motor Compensation Strategies in Children and Adolescents With Duchenne Muscular Dystrophy

Abstract

Duchenne Muscular Dystrophy (DMD), the most common form of muscular dystrophies, is characterized by progressive and generalized muscle weakness. The weakness of the trunk and other muscle groups leads these patients to perform motor compensation strategies to maintain their lower limb functionality for gait quality and for tasks such as getting up from a sitting position. In this cross-sectional observational study, we described and quantified trunk, gait, and sit-to-stand motor compensation strategies in different stages of this disease. Thirty-one ambulatory 5–18-year-old children and adolescents with a diagnosis of DMD, underwent cognitive assessment with the Mental Mini-Examination (MMSE) and motor assessment with the Vignos scale, Segmental Assessment of Trunk Control (SATCo-BR), Timed Up and Go test (TUG Test), and 10-m walk test. We found strong correlations between trunk and gait compensations, and identified motor compensation strategies characteristic of certain DMD classifications. Also, these lower limb and trunk compensations related to disease staging (Vignos) such that compensations were fewer for patients at relatively better disease staging.

Keywords

muscular dystrophy duchenne gait posture disability evaluation trunk

Bullet Points

Charcacteristic compensatory strategies are identified at each disease staging classification, and the number of compensatory strategies increases with disease progreesion

Trunk compensatory strategies are related to gait

Compensatory strategies influence the ability and quality of chair gait and lift functions.

Introduction

Duchenne Muscular Dystrophy (DMD) is a recessive genetic disease that is linked to the X chromosome and results from a mutation in the dystrophin protein gene (segment Xp 21). It has a degenerative character and presents with progressive and generalized muscle weakness (Brehm et al., 2014; Ganea et al., 2012; Hu & Blemker, 2015). This genetic alteration implies an alteration of the dystrophin protein production, responsible for maintaining sarcolemma integrity during cycles of muscle contraction and relaxation (Lim et al., 2017; Sackley et al., 2009; Walter & Reilich, 2017). The absence of dystrophin is responsible for susceptibility to muscle degeneration after repetition of movement patterns related to the maintenance of posture, mobility, and activities of daily living; therefore, motor patterns are different from age expectation in individuals with DMD (Birnkrant et al., 2018; Flanigan, 2012; Mah et al., 2014).

After acquiring gait functioning and with the evolution of the disease, patients with DMD adopt strategies to maintain body vertically. Among these are an enlarged stance base and an increase in balance difficulties of the pelvis and upper limbs. The increased balance difficulty of the pelvis is one of the most common characteristics of these patients’ gait, and it is related to weaknesses of the hip abductor muscles, which are then ineffective in stabilizing the pelvis during the stance to prevent a contralateral fall. The center of gravity shifts to the contralateral limb, causing imbalance, and the patient responds with an ipsilateral inclination of the trunk to maintain stability. This pattern repeats itself at every step and adds to broadening the base to maintain stability. Another very evident characteristic of the gait of patients with DMD is plantar flexion, generated by the imbalance between the plantar flexor and dorsiflexor ankle muscles. The plantar flexor muscles are stronger than the dorsiflexors. In addition, plantar flexion is a biomechanical adaptation necessary to maintain knee stability in the face of quadricep muscle atrophy. These patients remain ambulatory until muscle weakness and shortening begin to significantly alter their biomechanics (Iosa et al., 2014; Janssen et al., 2014; Ropars et al., 2016).

When relating these muscle shortenings and weaknesses and associated postural changes with gait, there can be tendon retractions and joint deformities by compensatory selection of synergistic movements of the hips, knees, and ankles that allow the individual to maintain function for as long as possible. These compensations and motor strategies, allow patients with DMD to maintain diverse functions with enormous muscle weakness (Baptista et al., 2014; de Carvalho et al., 2015). These changes are all related to each other, and to the generation of motor compensation strategies during activities of daily living.

In addition to these altered movement patterns during gait, patients with DMD present in an orthostatic position in which there is an anterior projection of the center of mass in relation to the individuals’ posture without the disease and without possible muscle shortening. Such projection characteristics of patients with DMD, therefore, promote an increase in falls during gait, and changes in the patterns of anticipatory adjustments of the trunk muscles (Baptista et al., 2014; de Carvalho et al., 2015; Martini et al., 2014).

Postural control is influenced by the neural system, and skeletal muscles are the first muscular system responsible for sensory information and the second system for producing the forces necessary to control body position. Muscle weakness and progressive body misalignment shown by patients with DMD alter trunk symmetry and the patterns of contraction of the axial and appendicular muscles. Thus, these patients present alterations in the activation of the synergist-agonist musculature, influencing the stability and functionality of the lower limbs, upper limbs, and head positioning. In addition, individuals with DMD have alterations in anticipatory postural control, which are present even before voluntary movement changes and that minimize imbalance caused by movements. All these changes are related to each other, generating compensatory movements (Hu & Blemker, 2015; Sá et al., 2017).

A question raised by past researchers is the degree to which weak trunk muscles influence lower limb functionality and gait quality of patients with DMD (Artilheiro et al., 2017; Martini et al., 2014; Sá et al., 2016). For the typically developing healthy individual, the influence of trunk control on gait has been widely studied with well-established intervention protocols (Mueller et al., 2016; Shahvarpour et al., 2015). However, the literature is scarce when assessing trunk control among patients with DMD and its influence on gait and sit-to-walk.

In this study, we sought to (a) quantify and describe the trunk, gait and sit-to-stand motor compensation strategies in patients at different DMD stage classifications; and (b) compare the number of motor compensation strategies in these disease stages. We defined a motor compensation strategy as compensatory movements adopted to perform functional activities due to muscle weakness in individuals with DMD. Our study hypothesis was that patients at more advanced stages of DMD would have a greater number of compensations when walking and getting up from a chair than would those at earlier disease stages.

Method

Study Type and Participants

This was a cross-sectional study design. We estimated a required participant sample size using the G*Power 3.1 program (Faul et al., 2009). Based on 0.80% power, an effect size of 0.5, and statistical significance set at p < .05, this calculation suggested a need for 21 participants for our planned one-way analyses of variance (ANOVA).

Participant inclusion criteria were: (a) a diagnosis of DMD as confirmed by muscle biopsy and/or genetic sequencing, (b) aged between 5 and 18 years, (c) underwent follow-up consultations at the Muscular Dystrophy Clinic of the University with a score ≥10 on the Mini Mental State examination (MMSE; Folstein et al., 1975; Voos et al., 2015) and (d) classification on the DMD disease staging scale, with a Vignos score ≤6 (Vignos et al., 1963). Participant exclusion criteria were cognitive, visual and/or hearing deficits that could prevent the application of our intended assessment tools. Additionally, we excluded patients with associated orthopedic and/or neurological diseases and those who had no independent gait.

Thirty-eight male participants withs DMD were selected. However, four were excluded (three males with DMD had orthopedic surgery within six months of data collection, two males had MMSE <10, and three males had associated autism). Thirty-one male participants participated in the study (M age =7.8, 3.4 years; M weight = 31.2, 8.7 kg; M height = 1.26, 0.2 meters).

This study was approved by the Research Ethics Committee of the University (Number: 1440/2016), according to Normative Resolution 466/12 of the National Health Council. Consent was obtained in writing from the parents/guardians of all children before their assessment. In addition, all children and adolescents signed the Free and Informed Assent Form,

Assessment Measures

Cognitive Assessment (MMSE)

We used the MMSE to evaluate these participants’ cognitive functioning. This instrument contains test items measuring temporal orientation, spatial orientation, memory, attention, calculation ability, recall of three words, language and visual-motor constructive capacity. Its maximum score is 30 points, with increasingly lower scores indicative of cognitive impairment (Bertolucci et al., 1994; Brucki et al., 2003), depending on the participant’s baseline condition. The MMSE was validated for the Brazilian population, and it has been recommended by the Brazilian DMD Consensus as a means of assessing cognitive performance among individuals with DMD (Araujo et al., 2018). For patients in this study, we used a 10-point cutoff, as proposed in a previous study in which individuals with this cutoff were able to perform the evaluations and understand simple verbal commands (Voos et al., 2015).

DMD Staging (Vignos Scale)

We performed motor assessment using the Vignos scale (Vignos et al., 1963) that assisted the identification of the clinical stage of each participant’s muscular dystrophy. The Vignos Scale is considered the gold standard for this purpose, with inter-observer classification consistency of 0.087 and intra-observer consistency of 0.92 (Florence et al., 1984). The scale provides classificatory data through the respondent’s performance of motor functions and the examiner’s grading of the disease in stages. Vignos scale scores range from 1 to 10, with higher scores reflective of poorer functional performance, as, for example, for (a) walking (Vignos ≤6) or (b) non-walking (Vignos ≥7) groups. In the present study, the researcher who classified the patients’ disease stage had 10 years of experience in using the Vignos scale.

Trunk Control

We had participants perform the Segmental Assessment of Trunk Control (SATCo), developed and validated by Butler et al. (2010) to assess trunk control in children with neuromotor disorders. The scale was translated and adapted to Brazilian Portuguese and was then called Avaliação Segmentar do Controle de Tronco (SATCo-BR) (Sá et al., 2017); it has been adapted for the population with muscular dystrophy, with the position of the upper limbs (ULs) placed at 45° to perform the tests (Sá et al., 2016). A suitable seat height and a pelvis-attached strap system were used to ensure that the pelvis remained in a neutral position. This tool considers the many sub-units that must be coordinated to achieve control in sitting posture. To define trunk control levels (head; upper, middle, and lower thoracic areas; upper, lower, and total lumbar regions), we considered the last level at which all three components were present (static, active, and reactive) (Butler et al., 2010; Sá et al., 2017). Inter-rater reliability was excellent for the total data set at 0.84, and intra-rater reliability was also excellent at 0.98 across all data sets and aspects of control (Butler et al., 2010); inter-rater agreement was very strong for the variables of trunk control level for dystrophinopathy (Sá et al., 2016).

Timed Up and Go Test (TUG Test)

The Timed Up and Go Test (TUG Test) was performed to assess the participants’ mobility and gait (Podsiadlo & Richardson, 1991). The TUG Test has been shown to be a valid and reliable method of assessing dynamic balance (Alkan et al., 2017; Wall et al., 2000). In this test, the patient was positioned sitting on a chair and leaning back. As soon as they received the start command, participants moved from a sitting to a standing position, walked three m, circled around the established mark, returned the three m walked, and then sat in the chair, leaning back again. The TUG test was recorded by two video cameras attached to two tripods. One camera was positioned in the side view and the other in the anterior view of the volunteers.

Considering the characteristics of this participant sample, we made an adaptation to the TUG Test. As patients with DMD have muscle weakness that causes them to collapse when sitting, we timed the task from the start command until the moment the patient turned to sit in the chair, thus excluding the time for sitting and leaning from the count. We analyzed standing up from a chair by observing the following body regions: foot, ankle, knee, hip, trunk, upper limbs and head, in the following stages of rising from the chair: (a) trunk flexion, (b) transfer weight and (c) trunk extension, based on the sit-to-stand from the chair test (FES-DMD; Hukuda et al., 2010) which was previously determined to reflect motor compensation strategies with excellent reliability (intraclass correlation coefficient [ICC] ≥ 0.91) and good reproducibility (ICC ≥ 0.89) (Hukuda et al., 2013).

Gait Assessment

Gait was further assessed by the 10-m walking test; in this case, the participants traveled 1.5 m to the first mark, 10 m between the marks and 1.5 m at the end of the second mark (McDonald et al., 2010). The 10-m walk test was filmed by a camera positioned in anterior view. Acceleration and deceleration distances of 1.5 m were set only to ensure test accuracy but were not considered when the video was analyzed.

For gait analysis, we used the footage of the 10-m walk test and the motor compensations strategies present in each of the body regions (foot, ankle, knee, hip, trunk, upper limbs, and head) and in each gait phase (contact initial, load response, medium stance, final stance, pre-swing, initial swing, mid-swing, and final swing). These were described in domain-4 of the Functional Evaluation Scale for DMD (FES-DMD-D4, that provides detailed observational kinesiological analysis of gait (Intra-class correlation coefficients ranged from acceptable [0.74] to excellent [0.99]) (de Carvalho et al., 2015). The FES-DMD aims to quantify motor strategies in specific activities, monitor and evaluate important changes in muscle synergies. It consists of four domains that assess performance during: Domain-1: sitting down and getting up from a chair; Domain-2: going up and down stairs; Domain-3: sitting and getting up from the floor; and Domain-4: gait. The FES-DMD-D4 provides detailed kinesiological analysis of gait, describing motor strategies over 10 m. In this domain, gait was evaluated in the frontal plane - with a physical space of approximately 10 m, in which the trunk and head motor strategies, waist dissociation and changes in the base of support were observed in all gait phases (de Carvalho et al., 2015, 2019).

Procedure

The order (with 5-min intervals between tests) evaluations of the previously reported tests were: cognitive (MMSE), DMD staging (Vignos), trunk control (SATCo), gait (TUG test) and walking 10 m. All evaluations were performed by a single professionally trained examiner.

To perform these individual assessments, we used two cameras, a Sony Hdr-cx405 Full HD Digital Zoom 350x + 32gb camcorder mounted on a Canon Nikon Sony professional photographic universal tripod (X-Zang manufacturer) and an installed camera. Cameras positioned in a side view and an anterior view of the participants. After all assessments, the videos of all participants were analyzed by the same examiner, which allowed identifying the individual’s trunk control level and number of motor compensations strategies during walking and sit-to-stand.

Statistical Analysis

We used the Shapiro Wilk test to verify the normality of the data distribution and the Levene test to verify homogeneity. For the number of gait motor compensations, the Levene test was 1.235 (p = 0.321), for the number of sit-to-stand motor compensations the Levene test = 1.203 (p = 0.334), and for the number of trunk compensation strategies the Levene test = 1.230 (p = 0.330). We performed descriptive analyses for the distribution of absolute and percentile frequencies of trunk, sit-to-stand chair, and gait motor compensation strategies. We used one-way analyses of variance (ANOVA) and Tukey’s post-hoc multiple comparison method to compare variables of interest across groups (i.e., numbers of compensations during the walking, sit-to-stand and trunk tests according to the Vignos classifications. For all statistical analyses, we used the Statistical Package for the Social Science (SPSS, Version 24). We set the statistical significance level at p < .05 for all analyses.

Results

It has been observed that 100% of patients with DMD who are at Vignos 1 stage of the disease have complete trunk control (i.e., static, dynamic, and reactive – all components of the control), while only 28% of patients at Vignos 5 have full trunk control. It is worth noting that the level of trunk control may vary with the staging of the disease, as 28% of patients with Vignos 5 have complete trunk control, while 57% have lower lumbar trunk control, and 14% have lower thoracic control (see Table 1).

Table 1.

Participant Characteristics Associated With Vignos Staging.

Vignos	Age	Trunk Control Level	Number of Patients
Vignos	M (SD)	Trunk Control Level	Number of Patients
1	8.6 (4.6)	Full	3
2	7.8 (3.4)	Lower lombar	1
2	7.8 (3.4)	Full	10
3	8.6 (5.5)	Lower lombar	1
3	8.6 (5.5)	Full	3
4	7.8 (2.2)	Lower lombar	4
4	7.8 (2.2)	Full	2
5	7.8 (1.7)	Lower thoracic	1
		Lower lombar	4
		Full	2

Note. M is mean; SD is standard deviation.

Table 2 shows that 33.3% of patients at Vignos 1 have one of the five motor compensations strategies observed when engaged in a sit-to-stand test from the chair. However, 100% of patients with Vignos 5 have four out of five motor compensation strategies. This frequency distribution indicates that the number of sit-to-stand motor strategies increases with disease progression.

Table 2.

Absolute Number and Percentile Distribution of Sit-to-Stand Chair Motor Compensations Strategies by Vignos Stages.

Motor compensations strategies	Vignos 1	Vignos 2	Vignos 3	Vignos 4	Vignos 5
Leg support to lift	1 (33.3%)	7 (63.6%)	4 (100%)	6 (100%)	7 (100%)
Chair support to lift	–	5 (45.4%)	2 (50%)	2 (33.3%)	7 (100%)
Wall support to lift	–	–	–	3 (50%)	7 (100%)
Need someone else’s help	–	–	–	3 (50%)	7 (100%)
Do not lock your knee	–	–	–	3 (50%)	7 (100%)

Patients classified as Vignos 1 and 2 have fewer motor compensations strategies than those at other stages, and motor compensation strategies increase gradually with disease progression, as shown in Table 3. However, in earlier stages, patients only compensate for shoulder elevation and head anteriorization that add to the head tilt and cervical extension in more advanced stages. Postural changes in sitting position such as thoracic rectification and pelvic anteversion also increase in frequency as the disease progresses.

Table 3.

Absolute Number and Percentile Distribution of Trunk Motor Compensations by Vignos Staging.

Trunk motor compensation strategies	Vignos 1 (%)	Vignos 2 (%)	Vignos 3 (%)	Vignos 4 (%)	Vignos 5 (%)
Anterior head	–	5 (45.4)	3 (75)	3 (50)	3 (42.8)
Tilted head	–	–	1 (25)	1 (16.6)	1 (14.2)
Round head	–	–	–	–	1 (14.2)
Cervical extension	–	3 (27.2)	4 (100)	3 (50)	4 (57.1)
Shoulder lift	1 (33.3)	6 (54.5)	2 (50)	5 (83.3)	4 (57.1)
Shoulder internal rotation	–	1 (9.09)	2 (50)	–	–
Thoracic rectification	–	1 (9.09)	–	1 (16.6)	3 (42.8)
Thoracic hyperkyphosis	–	2 (18.18)	1 (25)	1 (16.6)	2 (28.5)
Pelvic anteversion	–	1 (9.09)	–	–	3 (42.8)
Pelvic retroversion	–	6 (54.5)	3 (75)	4 (66.6)	2 (28.5)
Sacrum support in sitting position	–	3 (27.2)	2 (25)	1 (16.6)	–
Lumbar hyperlordosis	–	–	–	–	2 (28.5)
Arm drop					1 (14.2)

Motor compensation strategies reported in Table 4 represent the beginning of motor compensation strategies with medium and forefoot support, pelvic tilt and increased lateral dislocation in patients with Vignos 1. During the midstance and loading response gait phases, a decreased midstance and increased forefoot support as well as ankle inversion concomitant with disease progression are observed. Patients increase pelvic tilt and posterior trunk inclination for step maintenance in the terminal swing phase, motivated by the weakness of hip flexors and abductors. Hyperlordosis, head anteriorization as well as external support for gait performance and balance maintenance also increase gradually.

Table 4.

Absolute Number and Percentile Distribution of Gait Motor Compensations by Vignos Staging.

Gait Motor Compensation Strategy	Vignos 1	Vignos 2	Vignos 3	Vignos 4	Vignos 5
Inicial contact
Forefoot and midfoot support	2 (66.6%)	10 (90.9%)	3 (75%)	2 (33.3%)	2 (28.5%)
Forefoot support	–	–	1 (25%)	3 (50%)	5 (71.4%)
Foot inversion	1 (33.3%)	6 (54.5%)	2 (50%)	4 (66.6%)	5 (71.4%)
Knee flexion	–	5 (45.4%)	3 (75%)	3 (50%)	7 (100%)
Hip extension	–	1 (9.09%)	–	1 (16.6%)	–
Hip internal rotation	–	7 (63.6%)	4 (100%)	3 (50%)	6 (85.7%)
Loading response
Forefoot and midfoot support	–	9 (81.8%)	2 (50%)	2 (33.3%)	3 (42.8%)
Forefoot support	–	1 (9.09%)	1 (25%)	3 (50%)	4 (57.1%)
Foot inversion	1 (33.3%)	4 (36.3%)	1 (25%)	4 (66.6%)	5 (71.4%)
Knee extension	–	–	–	–	3 (42.8%)
Hip extension	–	1 (9.09%)	–	2 (33.3%)	1 (14.2%)
Hip internal rotation	–	7 (63.6%)	4 (100%)	2 (33.3%)	6 (85.7%)
Middle support
Forefoot and midfoot support	–	6 (54.5%)	2 (50%)	2 (33.3%)	5 (71.4%)
Forefoot support	–	1 (9.09%)	–	3 (50%)	2 (28.5%)
Foot inversion	–	4 (36.3%)	2 (50%)	4 (66.6%)	5 (71.4%)
Knee flexion	–	–	1 (25%)	2 (33.3%)	3 (42.8%)
Hip internal rotation	–	7 (63.6%)	3 (75%)	3 (50%)	6 (85.7%)
Terminal stance
Foot inversion	–	5 (45.4%)	–	4 (66.6%)	7 (100%)
Knee extension	–	–	1 (25%)	1 (16.6%)	2 (28.5%)
Hip internal rotation	–	7 (63.6%)	3 (75%)	4 (66.6%)	6 (85.7%)
Pre swing
Foot inversion	1 (33.3%)	4 (36.3%)	1 (25%)	2 (33.3%)	6 (85.7%)
Knee extension	–	–	–	1 (16.6%)	1 (14.2%)
Hip internal rotation	–	5 (45.4%)	3 (75%)	3 (50%)	7 (100%)
Initial swing
Hip flexion	–	1 (9.09%)	2 (50%)	3 (50%)	4 (57.1%)
Pelvis bascule	1 (33.3%)	7 (63.6%)	4 (100%)	4 (66.6%)	6 (85.7%)
Mid swing
Pelvis bascule	1 (33.3%)	5 (45.4%)	4 (100%)	4 (66.6%)	6 (85.7%)
Late swing
Plantar flexion	1 (33.3%)	3 (27.2%)	4 (100%)	4 (66.6%)	6 (85.7%)
Knee flexion	–	3 (27.2%)	2 (50%)	2 (33.3%)	4 (57.1%)
Hip internal rotation		6 (54.5%)	4 (100%)	3 (50%)	7 (100%)
Pelvis bascule	1 (33.3%)	6 (54.5%)	3 (75%)	5 (83.3%)	7 (100%)
Anterior trunk	–	2 (18.18%)	3 (75%)	4 (66.6%)	4 (57.1%)
Tilted trunk	–	1 (9.09%)	2 (50%)	–	2 (28.5%)
Round trunk	–	–	1 (25%)	–	2 (28.5%)
Anterior head	–	2 (18.18%)	1 (25%)	3 (50%)	6 (85.7%)
Tilted head	–	1 (9.09%)	2 (50%)	1 (16.6%)	1 (14.2%)
Round head	–	–	1 (25%)	–	3 (42.8%)
Cervical extension	-	1 (9.09%)	–	–	3 (42.8%)
Thoracic rectification	–	–	1 (25%)	1 (16.6%)	4 (57.1%)
Pelvic unevenness	–	–	3 (75%)	–	3 (42.8%)
Hyperlordosis	1 (33.3%)	4 (36.3%)	2 (50%)	5 (83.3%)	7 (100%)
Increased upper limb balance	1 (33.3%)	4 (36,3%)	2 (50%)	3 (50%)	5 (71.4%)
Increased side dislocation	2 (66.6%)	8 (72.7%)	3 (75%)	4 (66.6%)	6 (85.7%)
Posterior trunk inclination	–	1 (9.09%)	–	2 (33.3%)	3 (42.8%)
Support base increase	–	2 (18.18%)	3 (75%)	1 (16.6%)	5 (71.4%)
Wall support	–	–	–	1 (16.6%)	2 (28.5%)
Need someone else^’s help	–	–	–	–	1 (14.2%)

Table 4 shows two large groups verified during the observation of gait motor compensation strategies blocks. One group had plantar flexion, knee hyperextension, trunk posteriorization, head anteriorization and enlarged base; this group presented Vignos 4 and 5 classifications and with older ages; they remained functional for a longer period of life. Patients who used knee flexion and trunk anteriorization as motor compensatory strategies were younger in the same functional classification.

The analysis of variance for the Vignos classifications showed significant differences in the number of gait motor compensation strategies, F (4, 30) = 7.372, p ≤ 0.001), number of trunk motor compensation strategies, F (4, 30) = 3.563, p = 0.019, and number of sit-to-stand motor compensation strategies, F (4, 30) = 16.318, p ≤ 0.001. On Tukey’s test post hoc analysis, patients at Vignos 3 had a higher number of gait (p = 0.035) and trunk (p = 0.014) motor compensation strategies than patients at Vignos 1, indicating that the compensations for trunk and gait increased at Vignos 3 to maintain functionality. Patients at Vignos 5 presented higher number of compensations on all variables compared to those at Vignos 1: gait (p = 0.001), trunk (p = 0.042) and sit-to-stand (p = 0.001).

There was a difference in the number of sit-to-stand compensations strategies between patients at Vignos 1 and 4 (p = 0.011), and between Vignos 2 and 4 (p = 0.014), indicating that patients at Vignos 4 compensated more to perform the task. Patients at Vignos 5 also needed a greater number of compensations to complete the task compared to patients at Vignos 2 (p ≤ 0.001) and Vignos 3 (p ≤ 0.001).

Disucssion

In this study, we quantified and described the trunk, gait, and sit-to-stand motor compensation strategies of patients at different DMD disease staging classifications, and we compared the number of motor compensation strategies within these disease staging classifications. Our hypothesis that patients in more advanced stages of the disease would have greater numbers of compensations when walking and getting up from a chair was confirmed. This finding corroborated de Carvalho et al. (2015) and Ciafalonia et al. (2016), who established that motor compensatory strategies occurred according to disease progression and were related to each other, increasing in number and intensity with disease progression.

We observed that patients with lower Vignos classifications (better functional level) showed lower numbers of compensations during sit-to-stand compensations. Thus, patients with Vignos 1 presented leg support compensation when getting up from the chair compared to no compensation, in a neurotypical peer. The weakness in the knee, hip and trunk extensor muscles increased with disease progression, as for patients at Vignos classifications 3, 4, and 5, when patients leaned against the wall and asked for help to extend their knees and achieve orthostatic position. Previous studies (de Carvalho et al., 2019; Hukuda et al., 2017; Hu & Blemker, 2015) also described increased compensatory strategies during the sit-to-stand task, related to muscle weakness and disease progress, but they did not report which strategies were performed at each stage of disease. Another fact observed in our study and reported in past literature (Hukuda et al., 2017; Hu & Blemker, 2015) was of increased movement and support by upper limbs according to disease progression; at Vignos 5, patients demonstrated the need for arm support throughout the activity.

Hu & Blemker (2015) and Hukuda et al. (2017) reported that muscle weakness was more evident in the proximal musculature that moves to the distal musculature, relating the degeneration pattern to greater eccentric contraction. Thus, there was support for therapies that guide minimization of eccentric contractions to delay muscle injuries and functional losses. We observed that the level of trunk control did not necessarily worsen with disease progression, since there were individuals at both Vignos 1 and 5 who had total trunk control. This finding points to the heterogeneity of patients with DMD and the need for individualized assessments and protocols for each patient, to guide optimal individualized therapeutic strategies. However, although they have total trunk control, the number of compensatory motor strategies may be different, and we noticed that these compensatory motor strategies increased with disease progression.

We observed, during assessments of trunk motor compensation strategies in accordance with the Vignos classifications, that the compensations increased in number and severity as the disease progressed. Patients presented elevation of shoulder and anterior head as a response to abdominal muscle weakness in earlier stages. Patients used their heads to stay erect with the deficit of abdominal muscle contraction, assisted together by their upper limbs to accomplish the task. Disease progression and muscular degeneration caused head inclination and cervical extension to be added to the first compensations. At this stage, individuals compensated for the trunk muscle weakness with movements of the head, cervical region, and shoulder girdle. As the disease progressed, in addition to the compensations described, they also compensated for thoracic hyperkyphosis and pelvic retroversion generated by the weakness of the hip and trunk extensor muscles, common in these patients. Patients at Vignos 5 replaced compensations for hyperkyphosis and retroversion with thoracic rectification and lumbar hyperlordosis in later stages of the disease. This compensation was widely used during gait and generated shortening that made it impossible to disappear at times when it should not exist, such as when the patient sat. This change moved from dynamic compensation to fixation. Although description of trunk compensations at different stages of the disease have been scarce, Artilheiro et al. (2017), Maciel et al. (2021) and Martini et al. (2014) reported compensatory movement progression with disease evolution, corroborating our findings and demonstrating the importance of assessing compensatory strategies and their consequences in patients with DMD.

The assessment of compensations during gait activity, compared with the Vignos scale, demonstrated the beginning of compensations with medium foot support, pelvic tilt and increased lateral displacement when considering Vignos 1. These compensations were linked to weaknesses of the anterior tibial, extensor and hip abductor muscles. New compensations were added to these as the disease progressed. Support was made in the forefoot, suggesting increased anterior tibial weakness and shortening of the calcaneal tendon; the ankle was inverted, and the knee was hyperextended, as the weakness of the dorsiflexors and knee extensors no longer held it neutral when standing upright. In this case, knee extension and plantar flexion performed a bone lock that contributed to balance at the patient’s center of mass. We observed an increased pelvic tilt and ipsilateral and posterior trunk inclination for the maintenance of the step in the terminal swing phase due to weakness of the hip flexor and abductor muscles. Changes followed the gradual increase in hyperlordosis, base support, head anteriorization, and external support to maintain functionality and stability.

Goudriaan et al. (2018) reported findings similar to ours when discussing the decrease in ankle dorsiflexion during the swing phase and the decrease in knee extension and dorsoflexion in the loading response phases. These authors related these findings to dorsoflexor weakness and shortening in plantar flexors, describing that patients underwent knee hyperextension and plantar flexion in order to compensate for progressive muscle weakness in the quadriceps and dorsoflexors, the biomechanical positioning, and anteriorized center of mass.

Baptista et al. (2014) described, as first compensations, increased base support, lumbar hyperlordosis, knee hyperextension, anterior pelvic tilt and consequent anteriorization of the center of mass. Goudriaan et al. (2018) and Baptista et al. (2014) pointed out that anteriorization of the center of mass initiated a compensatory strategy, that included lumbar hyperlordosis and posterior trunk inclination. The authors also reported that patients with DMD presented decreased ground reaction force and projected force anteriorly to the knee in the gait stance phase in response to weakness of the hip extensors, such as the gluteus maximus, and knees, such as the quadriceps; this weakness led to increased hip and knee flexion in the loading response phases in the early stages of the disease. These authors also stated that knee flexion ceased to occur with disease progression, and the patient performed hyperextension to keep walking with a lower fall risk.

The gait compensations for patients with DMD widely described in the literature are plantar flexion, knee hyperextension, trunk posteriorization, head anteriorization and broad base. Such motor compensatory strategies could be evidenced in gait assessment in this study, while we also observed a group of patients that did not evolve in compensations; these individuals maintained motor compensatory strategies like the early stages of the disease with knee flexion and trunk anteriorization. Such patients had larger functional deficits at younger ages. These motor compensation strategies were inadequate to the presented muscle weakness, requiring muscle strength from structures that were too weak to maintain eccentric contraction for long periods. This choice was less frequent and may have been motivated by early shortening or even inadequate biomechanical actions. This finding should be explored in future studies, as it suggests that effective motor compensation strategies may represent a better functional level for longer disease duration. No similar reports were found in the literature. On the other hand, prolonged eccentric contraction has caused muscle damage, with subsequent glycoprotein tissue deposition and muscle weakness increase (de Carvalho et al., 2019; Hu & Blemker, 2015; Lim et al., 2017; Sackley et al., 2009; Walter & Reilich, 2017).

In this study, some patients presented knee flexion and trunk anteriorization in advanced stages; these were compensations that required sustained eccentric contractions to maintain standing posture. The strategies described may accelerate disease progression. Based on findings of motor compensatory strategies, Ropars et al. (2016) proposed that health professionals seek ways to improve stability and movement pattern during gait to reduce muscle hyperactivity and early degeneration. Our findings establish a similar disease progression path to that of Ropars et al. (2016) and suggest a need for further studies to identify (a) the reason for the specific motor compensation strategies chosen by the patients, and (b) the therapy direction needed to avoid muscle hyperactivity and early degeneration.

The performance of a given motor activity depends not only on muscles and joint integrity, but also on the ability to develop motor strategies that minimize dysfunction. Using motor strategies, patients with DMD can preserve their independence longer, even in the face of muscle weakness (Martini et al., 2014), as was seen in this study. For effective rehabilitation, the motor performance of patients with DMD must be better understood (Nizamis et al., 2020). In clinical practice, performance assessments such as the TUG test and walking 10 m should be complemented with assessments of the motor strategies employed by these patients in their daily activities; this will allow the identification of the moment when these strategies increase, as well as when they are no longer efficient.

Limitations and Directions for Further Study

A limitation of this study was the heterogeneity of our sample, both in age and DMD severity. While our study was large enough to generate sufficient statisical power, it was not large enough to permit broad generalization of these results. Thus, future studies with larger and more diverse patients are needed to permit age and sex group classifications and a fuller understanding of sociocultural environmental factors in the development of various disease stages. Larger studies might also permit further analyses of DMD groups divided by the type of DMD mutation.

Conclusion

Motor compensatory strategies performed by patients with DMD in the trunk, gait and sit-to-stand tasks provide information for clinical practice as they identify moments of functional loss and even choices of motor compensation strategies that mitigate the stress caused by muscle hyperactivity. Our findings in this study provide data for clinicians about the motor behavior of patients with DMD in terms of trunk control, time of execution of functions and quality of movements. These data can help to establish, through disease staging, the moments at which compensatory strategies begin and later become inefficient. We also described the types of compensations that can reduce the eccentric contraction requirement and the injury resulting from selecting inappropriate compensatory strategies. Finally, data here may contribute to characterizing these patients more accurately. We observed that trunk control is very similar among ambulatory patients and does not present significant differences in the execution times of tasks and in the number of compensatory strategies. Further cross-validation research is needed, especially with larger and more diverse participants.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval

The study approved by the Research Ethics Committee of the Federal University of São Paulo (n: 1440/2016).

ORCID iD

Cristina Dos Santos Cardoso De Sá

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