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Effect of Plantar Flexor Muscle Strengthening on the Gait of Children With Idiopathic Toe Walking

A Study Protocol

de Oliveira, Vanessa Gonçalves Coutinho PT; Arrebola, Lucas Simões PT, MSc; de Oliveira, Pedro Rizzi PT; de Sá, Cristina dos Santos PT, PhD; Yi, Liu Chiao PT, PhD

doi: 10.1097/PEP.0000000000000650
PROTOCOL
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Purpose: To evaluate the effect of plantar flexor strengthening associated with conventional physical therapy treatment in participants with idiopathic toe walking.

Methods: Thirty participants, of both sexes diagnosed with idiopathic toe walking, aged 5 and 11 years, will be recruited and randomized into 2 groups: the control group, who will undergo gait training, triceps surae muscle stretching, anterior tibial muscle strengthening, and motor sensory training, and the intervention group, who will undergo the same training as the control group and, additionally, triceps surae muscle strengthening. The intervention will be performed twice a week for 8 weeks. The participants will undergo a 3-dimensional gait kinematic analysis, passive amplitude of dorsiflexion movement, isometric dynamometry of the anterior tibial and triceps surae muscles, motor coordination, quality of life, and perception of the parents regarding the equinus gait at baseline and at the end of treatment. Quality of life will be reevaluated during a 24-week follow-up.

To evaluate the effect of plantar flexor strengthening associated with physical therapy treatment in children with idiopathic toe walking.

Department of Human Movement Science (Ms V. G. C. de Oliveira, Messrs Arrebola and P. R. de Oliveira, and Drs de Sá and Yi), Federal University of Sao Paulo, Santos, Sao Paulo, Brazil; Department of Physical Therapy (Ms V. G. C. de Oliveira and Messrs Arrebola, and P. R. de Oliveira), State Public Server Medical Assistance Institute of São Paulo, São Paulo, Sao Paulo, Brazil.

Correspondence: Liu Chiao Yi, PT, PhD, Department of Human Movement Science, Federal University of Sao Paulo, Rua Silva Jardim 136, Santos, Sao Paulo, Brazil- CEP 11015-020 (liu.unifesp@gmail.com).

The authors declare no conflicts of interest.

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INTRODUCTION

Idiopathic toe walking (ITW) is a condition that affects participants aged 5 years and older, with a prevalence of 4.9% and unknown etiology. It is characterized by a spontaneous gait pattern in plantar flexion, in which the heel does not touch the floor in the initial contact of the support phase, and control of the gait pattern when requested.1,2 Gait pattern in plantar flexion is considered physiological during the first 3 years of life and abnormal after this age.3 Idiopathic toe walking is considered a differential diagnosis when neurological, orthopedic, and psychiatric causes are discarded.3

Participants with ITW have some characteristics similar to participants with diplegic cerebral palsy (CP), such as premature activation of plantar flexors at the end of the balance phase and overlap of the activity of this muscle group on the dorsiflexors.4,5 In addition, type I fibers prevail in the muscle composition of the triceps surae (TS), similar to that observed in the participants with CP.6 However, the anterior tibial (AT) activity during gait is similar to the pattern observed in participants who are typically developing.4,5 Gait can be described as the movement of an inverted pendulum, in which there are exchanges between potential and kinetic energy as an energy conservation mechanism.7 Participants with CP have a neuromotor dysfunction that changes muscle tone, muscle strength, and tendon reflexes, such that the plantar flexors do not provide enough energy during the toe-off phase, changing the physiological pendulum pattern of the gait. Thus, a functional displacement requires the generation of an alternative energy form, depending on the dynamic resources available, using the elastic energy accumulated from the TS to obtain mechanical advantage for displacement through the “spring” mechanism. This is how the initial gait contact in plantar flexion (equinus gait) occurs, and the production of connective tissue increases during the first few years of a participant's life as a result of reduced muscular strength.8

The equinus gait pattern gradually leads to ankle rigidity and plantar flexor contracture,8,9 as well as postural compensations such as anterior pelvic tilt and external hip rotation during gait. As a result, increased tibial twisting, ankle and foot pain, and sensory dysfunction may result in a balance deficit.10 Regardless of whether the primary cause for equinus gait is orthopedic or neurological, premature activity of plantar flexors is associated with weakened plantar flexor muscles.11

Idiopathic toe walking can be treated by serial plaster casting, botulinum toxin administration, TS muscle stretching surgical procedures, and physical therapy. Physical therapy includes motor control training, AT muscle strengthening, plantar flexor muscle stretching, and gait training on the heels by active dorsiflexion.12 Previous evidence has shown that such therapies may be beneficial. However, a recent systematic review3 showed that the studies described in the literature have low methodological quality and small sample sizes.

Current treatments aim to correct the equinus foot posture; however, none of the studies used an intervention based on its etiology, that is, early activation and weakness of the TS muscle. Thus, investigating the effect of strengthening the plantar flexor muscle in addition to conventional conservative treatment would be essential to reestablish the physiological pendulum pattern in the gait of participants with ITW. Therefore, the objective of this study is to verify the effect of plantar flexor muscle strengthening in participants with ITW, in addition to a conventional physical therapy program consisting of TS muscle stretching, AT muscle strengthening, gait training, and sensory motor training.

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METHODS

Study Design

This is a blind, randomized, and controlled clinical trial with 2 groups.

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Approval and Registration

The study design with procedures and the informed consent form were approved by the Ethics Committee of the Federal University of São Paulo Institute under number 2.178.996 on July 19, 2017.

This study was designed following the indications of the CONSORT13 and the Template for Intervention Description and Replication (TIDieR) Checklists.14 The sample will include participants from the pediatric orthopedic out participant clinic of a tertiary hospital in the city of São Paulo. Participants will be treated by a pediatric physiotherapist experienced in the area at the pediatric physical therapy out participant clinic of the same hospital. This study was prospectively registered in the Brazilian Clinical Trials Registry (www.ensaiosclinicos.gov.br/) and approved under RBR-7qnffg.

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Sample Calculation

The sample size was calculated considering variable ankle dorsiflexion as the primary end point, according to the mean difference of 6.29 and standard deviation of 3.85 found by Williams et al.15 An α level of 5% and power of the test of 95% were used. A total of 15 participants per group will be necessary considering an estimated sample loss of 20%, an α level of 5%, and power of the test of 95%.

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Participants

Thirty participants of both sexes diagnosed with ITW and aged between 5 and 11 years will participate. According to the criteria by Kuijk et al3 and Ruzbarsky et al,2 the participants must have bilateral plantar flexion during gait.

The exclusion criteria are neurological, cognitive, and orthopedic disorders associated with equinus gait; structural ankle deformity (not reaching the neutral position of the ankle passively); and locomotor surgery or botulinum toxin administration in the plantar flexor muscles in the last 12 months.

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Evaluation and Blinding Procedures

The participants will be referred to the physical therapy center. If the participant is considered eligible, the evaluator, who is masked to participant allocation and treatment, will perform the initial evaluation prior to randomization.

Parents or legal guardians will be informed of the study objectives and schedule. If they agree with the proposal, they will be asked to sign the informed consent form.

Three independent assessors will perform the assessments. The first will be responsible for applying the questionnaires, the lunge test, the muscle strength measure, and the Körper koordinations Test für Kinder (KTK) tests for placing the markers and filming the participants.

The other 2 assessors will be responsible for the kinematics analyses. The interreliability will be evaluated by comparing the data (video analysis) between 2 independent assessors and the same evaluator with an interval of 14 days for intrarater reliability.

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Primary Outcome

The primary outcome will be the active ankle dorsiflexion angle evaluated by kinematic gait analysis at the eighth week after randomization.

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Secondary Outcome

Secondary outcomes will be the angular kinematic variables of the hip and the knee, passive ankle dorsiflexion angle, dorsiflexor and plantar flexor muscle strength, pain, motor coordination, quality of life, and the parents' perception of frequency of equinus gait valuated at the eighth week after randomization. Quality of life and the parents' perception of frequency of equinus gait will be reevaluated on the sixth month after randomization.

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The Evaluation Instruments

Muscle Strength Evaluation

The strength of the TS and AT muscles will be evaluated using a manual dynamometer (Lafayette Instrument, Lafayette, Indiana). The participant will be placed on the stretcher in dorsal decubitus position, with full extension of the hip and the knee. To stabilize the lower limb, a belt will be placed over the supramalleolar region. The evaluator will place the manual dynamometer perpendicular to the stretcher16 TS muscle strength will be measured by positioning the dynamometer in the plantar region of the foot on the metatarsal head. The participant will be asked to apply maximum plantar flexion force against the dynamometer. To evaluate the AT muscle, the evaluator will position the dynamometer in the dorsal foot of the participant, near the metatarsophalangeal joint, while the participant will be encouraged to apply maximum dorsiflexion force.16 A submaximal contraction will be applied prior to the evaluation for familiarization with the test, and, subsequently, 3 maximum contractions will be applied for each muscle evaluated, with a 1-minute rest between contractions. The mean of the 3 measurements will be considered the final value. The isometric forces will be measured in kilograms and normalized for each volunteer using the formula: force kg/body mass index.17

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Kinematic Gait Analysis

To perform the kinematic analysis, a 6-camera 3-dimensional motion system (Vicon Vero 1.3) will be used at 240 Hz and the Software Nexus 2 will be used for analysis.18,19

The participants will be evaluated wearing swimsuits. Fifteen reflective markers will be placed bilaterally on the skin over the following bony prominences: lateral region of the fifth metatarsal head, lateral malleolus, lateral joint of the knee, greater trochanter of the femur, anterior superior and posterior superior iliac spine, and first sacral vertebra (20). In addition, clusters will be used on the lateral face of the thigh and leg. Clusters will consist of 4 non-collinear markers arranged on a rigid base, and will be attached to the participant by velcro straps.

The participants will be instructed to walk at a self-selected speed, barefoot, in a straight line, attempting to complete 8 cycles. The predelimited path is 10 m long and 2 m wide.

The angular kinematic variables in the sagittal plane will be as follows:

  • Ankle: maximum initial extension of the ankle (foot flattening), maximal ankle flexion, maximum final extension of the ankle (toes off), and sagittal range of motion (ROM) of the ankle (defined as the maximum flexion value subtracted from the maximum extension value at the end of the support phase).
  • Knee: maximum initial knee flexion, maximum knee extension, maximum knee flexion, and sagittal ROM of the knee (defined as the maximum extension value subtracted from the maximal flexion value).
  • Hip: maximum initial hip flexion, maximum hip extension, and sagittal ROM of the hip (defined as the maximum flexion value subtracted from the maximum extension value at the end of the support phase).
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ROM of Passive Ankle Dorsiflexion

The lunge test will be used to measure the ROM of ankle dorsiflexion. The participant will be instructed to perform the dorsiflexion movement in a closed kinetic chain, without losing the contact of the knee with the wall and the heel with the ground. A flexometer will be placed on the lateral side of the volunteer's leg. When the maximum dorsiflexion is reached, the examiner will read the flexion angle.20

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Quality of Life

The generic Pediatric Quality of Life Inventory version 4.0 (PedsQL 4.0) questionnaire will be used to evaluate quality of life. It was validated and translated for the Brazilian population,21 and its use was authorized by the PROVIDE Web site under the number 117 527. The generic PedsQL 4.0 questionnaire has 23 items distributed among 4 domains: the physical dimension, with 8 items, and emotional, social, and school dimensions (with 5 items each). The questionnaire can be applied to participants and teenagers from 2 to 18 years of age and has adapted forms for each age group. Parents or guardians will also complete a form with their perception of the participant's quality of life. The questions have a 5-level response scale (0 = never a problem, 1 = almost never a problem, 2 = sometimes a problem, 3 = often a problem, and 4 = almost always a problem). The scores obtained in each domain will be divided by the total number of questions in the domain. The total scores for each domain will be added. The closer the score to 100, the better the quality of life. In contrast, the closer the score to 0, the worse the quality of life.21,22

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Motor Coordination and Balance

A body coordination test for participants (KTK) will be used to evaluate motor coordination and balance. This test can be applied to participants and teenagers from 5 to 14 years of age,23 being widely used in the Brazilian population. These are distributed to 4 tasks:

Balance beam: The participant will be instructed to walk backward on a beam without losing balance, trying to reach the end of it. This test will be conducted on 3 beams, the first measuring 3.60 m × 6 cm, the second 3.60 m × 4.5 cm, and the third 3.60 m × 3 cm.

Monopodal jumps: The participant will be instructed to jump on 1 foot on a 5-cm high foam mat. Depending on the participant's performance, other mats with the same height will be added, up to a maximum of 10 mats. The participant will hop, alternating the lower limbs.

Side jumps: The participant will jump on a piece of wood measuring 60 × 4 × 2 cm, from one side to the other, as fast as possible for 15 seconds. The participant will jump using both lower limbs.

Transfer on platforms: The participant will move laterally between 2 boards (25 × 25 × 1.5 cm), the greatest number of times in 20 seconds.24

The final result of each task will be marked in a system of gross values and converted into a motor quotient (MQ) according to the participant's sex and age. The global MQ classifies gross motor development into the following categories: low (first tercile, 65<MQ<106), normal (second tercile, 107<MQ<118), and high (third tercile, 119<MQ<140).24

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Parents' Perception on How Often the Participant Walks on Toes

Parents will be asked how often they see their participant walking on toes, rating the frequency at 0%, 25%, 50%, 75%, or 100% of the time (or intermediate values between these percentages). They will be asked about this perception at baseline, posttreatment, and follow-up.12

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The Wong Baker Faces Pain Rating Scale

The analog scale consists of 6 expressions, ranging from painless to unbearable pain, where “no Hurt” 0 = no pain and “Hurts Worst” 5 = unbearable pain.25

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PARTICIPANT RANDOMIZATION

After the baseline evaluation, the participants will be referred to a researcher who was not involved in their recruitment, evaluation, or treatment. Randomization will be conducted through a random numerical table previously generated by the Excel software. These numbers will be allocated in the order obtained in sealed opaque envelopes, and the participants will be distributed by an independent collaborator.

The participants will be allocated into 2 groups and subsequently undergo the following interventions (Figure and Table).

Fig

Fig

TABLE

TABLE

Control group: TS muscle stretching, AT muscle strengthening, gait training, and sensory motor training.

Intervention group: The same procedures as those of the control group, in addition to TS muscle strengthening.

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STATISTICAL ANALYSIS

The data will be analyzed using the R software for Windows version 3.1.1 by a researcher masked to randomization. The descriptive data will be the mean (standard deviation) or median (interquartile range), as indicated. The variables will be analyzed according to the intention-to-treat principle; if there are losses, the missing data will be treated using multiple data imputation methods and sensitivity analyses.

The 2-way repeated-measures analysis of variance will be used to evaluate preintervention behavior, the quality of life and the parents' perception of frequency of equinus gait on the sixth-month follow-up, and differences between the groups according to the nature of data distribution. To do so, we will evaluate the assumptions of the methods (normality and homogeneity) through the visual inspection of histograms and box plots, comparison of mean and median values, and the Kolmogorov-Smirnov and Levene tests, respectively. If the data do not present symmetric distribution, we will consider logarithmic or exponential transformation for the data set. If after the transformations the asymmetric distribution remains, we will use the nonparametric tests with the gross data (without transformation).

An α level of 0.05 will be used for statistical tests. To confirm the relevance of the results, the effect size Cohen d will be measured considering 0.00 to 0.49 a small effect, 0.50 to 0.79 a medium effect, and 0.80 a large effect.

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DISCUSSION

To date, the main focus of ITW treatments is to stretch the TS muscle.3 The objective of this study is to verify the effect of adding plantar flexor muscle strengthening to the conventional physical therapy protocol.

The theoretical basis for proposing this treatment is the assumption of plantar flexor muscle weakness as a contributing factor for the equinus gait in participants with ITW. Some points that would explain this theoretical basis would be as follows:

  1. Morphologically, the muscle fibers of the TS muscles of these participants are predominantly type 1, whereas under normal conditions, there would be an equally proportional distribution of the 2 types of fibers. In addition, there are atrophic muscle fibers with nonspecific esterase and myopathic activities and type I muscle fibers that are smaller than type II,6 suggesting abnormal muscle activity, similar to that observed in participants with CP.
  2. The evaluation of surface electromyography shows premature activity of the gastrocnemius muscles in the balance phase compared with that in participants who are typically developing, like in participants with spastic diplegia.4 The gait of participants with diplegic and hemiplegic CP is characterized by the hindered exchange between potential and kinetic energy, resulting in equinus gait and increased vertical displacement of the center of mass, which makes the gait similar to a running pattern. These participants present decreased strength during the push off phase of gait and plantar flexion in the initial contact phase, which can be considered an adaptation that allows the use of soft tissue rigidity to recover elastic energy and become a “spring mass,”26 which is consequently more functional.8 This theory was applied to the ITW population due to morphological similarities found in muscle biopsy6 and electromyographic activity patterns.4

A recent computer simulation evaluated the effect of plantar flexor and dorsiflexor muscle weakness (reduction of maximal isometric force) in participants who are typically developing and showed increased activation of the weakened muscles as the main compensatory strategy and increased rigidity and decreased electromyographic activity as muscle strength decreased.27 These results endorse the theory of our study.

The key point of this study is to verify the effects of TS muscle strengthening in participants with ITW. However, the physical therapy treatments described to date have also been included, since these treatments reduce ankle dorsiflexion ROM and sensorimotor alterations of participants.12 Therefore, these strategies are also considered important in the rehabilitation of this population. To date, no randomized clinical trial has tested the effectiveness of conservative physical therapy treatment for this population. In addition, there are only the following 4 clinical trials on ITW treatment: 2 tested the effect of botulinum toxin administration,12,28 1 tested the short-term effect of whole-body vibration on the gait of participants with ITW,29 and 1 reported on the use of orthoses.30 Other studies are cross-sectional observational studies. Therefore, the findings of this study can expand treatment alternatives for these participants.

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REFERENCES

1. Engstrom P, Tedroff K. The prevalence and course of idiopathic toe-walking in 5-year-old participants. Pediatrics. 2012;130(2):279–284. doi:10.1542/peds.2012-0225.
2. Ruzbarsky JJ, Scher D, Dodwell E. Toe walking: causes, epidemiology, assessment, and treatment. Curr Opin Pediatr. 2016;28(1):40–46.
3. Kuijk A, Kosters R, Vugts M, Geurts A. Treatment for idiopathic toe walking: a systematic review of the literature. J Rehabil Med. 2014;46:945–957.
4. Policy JF, Torburn L, Rinsky LA, Rose J. Electromyographic test to differentiate mild diplegic cerebral palsy and idiopathic toe-walking. J Pediatr Orthop. 2001;21(6):784–789.
5. Kalen V, Adler N, Bleck EE. Electromyography of idiopathic toe walking. J Pediatr Orthop. 1986;6(1):31–33.
6. Eastwood DM, Dennett X, Shield LK, Dickens DR. Muscle abnormalities in idiopathic toe-walkers. J Pediatr Orthop B. 1997;6(3):215–218.
7. Kuo AD, Donelan JM. Dynamic principles of gait and their clinical implications. Phys Ther. 2010;90(2):157–174.
8. Fonseca T, Holt KG, Fetters L, Saltzman E. Dynamic resources used in ambulation by participants with spastic hemiplegic cerebral palsy: relationship to kinematics, energetics, and asymmetries. Phys Ther. 2004;84(4):344–358.
9. Holt KG, Obusek JP, Fonseca ST. Constraints on disordered locomotion: a dynamical systems perspective on spastic cerebral palsy. Hum Mov Sci. 1996;15:177–202.
10. Williams CM, Tinley P, Rawicki B. Idiopathic toe-walking: have we progressed in our knowledge of the causality and treatment of this gait type? J Am Podiatr Med Assoc. 2014;104(3):253–262.
11. Schweizer K, Romkes J, Brunner R. The association between premature plantarflexor muscle activity, muscle strength, and equinus gait in participants with various pathologies. Res Dev Disabil. 2013;34(9):2676–2683.
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13. Schulz KF, Altman DG, Moher D; CONSORT Group. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. BMJ. 2010;340:c332.
14. Hoffmann TC, Glasziou PP, Boutron I, et al Better reporting of interventions: template for intervention description and replication (TIDieR) checklist and guide. BMJ. 2014;348:g1687.
15. Williams CM, Michalitsis J, Murphy A, Rawicki B, Haines TP. Do external stimuli impact the gait of participants with idiopathic toe walking? A study protocol for a within-subject randomised control trial. BMJ Open. 2013;3(3):pii: e002389.
16. Mentiplay BF, Perraton LG, Bower KJ, et al Assessment of lower limb muscle strength and power using hand-held and fixed dynamometry: a reliability and validity study. PLoS One. 2015;10(10):e0140822.
17. Wren TA, Engsberg JR. Normalizing lower-extremity strength data for participants without disability using allometric scaling. Arch Phys Med Rehabil. 2007;88(11):1446–1451.
18. Eichelberger P, Ferraro M, Minder U, Denton T, Blasimann A, Krause F, Baur H. Analysis of accuracy in optical motion capture–A protocol for laboratory setup evaluation. J Biomechanics. 2016;49(10):2085–2088.
19. Mehl J, Otto A, Comer B, Kia C, Liska F, Obopilwe E, Beitzel K, Imhoff AB, Fulkerson JP, Imhoff FB. Repair of the medial patellofemoral ligament with suture tape augmentation leads to similar primary contact pressures and joint kinematics like reconstruction with a tendon graft: a biomechanical comparison [published online ahead of print August 13, 2019]. Knee Surg Sports Traumatol Arthrosc. doi: 10.1007/s00167-019-05668-z.
20. Powden CJ, Hoch JM, Hoch MC. Reliability and minimal detectable change of the weight bearing lunge test: a systematic review. Man Ther. 2015;20(4):524–532.
21. Klatchoian DA, Len CA, Terreri MTRA, et al Qualidade de vida de crianças e adolescentes de São Paulo: confiabilidade e validade da versão brasileira do questionário genérico Pediatric Quality of Life Inventory™ versão 4.0. J Pediatr (Rio J). 2008;84(4):308–315.
22. Varni JW, Seid M, Kurtin PS. PedsQL 4.0: reliability and validity of the Pediatric Quality of Life Inventory version 4.0 generic core scales in healthy and participant populations. Med Care. 2001;39(8):800–812.
23. Vandorpe B, Vandendriessche J, Lefevre J, et al The Körper koordinationsTest für Kinder: reference values and suitability for 6-12-year-old participants in Flanders. Scand J Med Sci Sports. 2011;21(3):378–388.
24. Ribeiro ASC, David AC de, Barbacena MM, Rodrigues ML, França NM de. Teste de Coordenação Corporal para Crianças (KTK): aplicações e estudos normativos. Motricidade. 2012;8:40–51.
25. Wong DL, Baker CM. Pain in participants: comparison of assessment scales. Pediatr Nurs. 1988;14(1):9–17.
26. Geyer H, Seyfarth A, Blickhan R. Compliant leg behaviour explains basic dynamics of walking and running. Proc Biol Sci. 2006;273(1603):2861–2867.
27. Fox AS, Carty CP, Modenese L, Barber LA, Lichtwark GA. Simulating the effect of muscle weakness and contracture on neuromuscular control of normal gait in participants. Gait Posture. 2018;61:169–175.
28. Sätilä H, Beilmann A, Olsén P, Helander H, Eskelinen M, Huhtala H. Does botulinum toxin a treatment enhance the walking pattern in idiopathic toe-walking? Neuropediatrics. 2016;47(3):162–168.
29. Williams CM, Michalitsis J, App Sc B, Murphy AT, Rawicki B, Haines TP. Whole-body vibration results in short-term improvement in the gait of participants with idiopathic toe walking. J Participant Neurol. 2016;31(9):1143–1149.
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Keywords:

biomechanical phenomena; equinus foot; muscle strength; participant; physical therapy

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