Pediatrics International (2015) 57, 92–97
Effect of muscle weakness distribution on balance in neuromuscular disease Pınar Kaya,1 I˙pek Alemdarog˘lu,3 Öznur Yılmaz,1 Ays¸e Karaduman1 and Haluk Topalog˘lu2 1 Physiotherapy and Rehabilitation Department, Faculty of Health Sciences, 2Department of Pediatric Neurology, I˙hsan Dog˘ramacı Children’s Hospital, Faculty of Medicine, Hacettepe University, Ankara and 3Physiotherapy and Rehabilitation Department, Faculty of Health Sciences, Bezmialem Vakıf University, Istanbul, Turkey Abstract
Background: To assess balance and identify the effects of muscle weakness distribution on balance in children with different neuromuscular diseases. Methods: Forty ambulant, pediatric patients with neuromuscular disease were enrolled in the study. Patients were separated into two groups according to muscle weakness distribution as group 1 (proximal) and group 2 (distal). Demographic data were recorded. Functional level (Brooke lower extremity functional classification), muscular strength (manual muscle testing), balance (pediatric functional reach test [PFRT], timed up-and-go test [TUGT], stabilometric platform) and functional performance (6 min walk test [6MWT]) were assessed. Results: Group 1 consisted of 20 Duchenne muscular dystrophy patients, and group 2, of 20 neuropathy patients. The total lower, upper limbs and trunk muscles muscle strength (P < 0.05); forward and right side reach subsections of the sitting position, and PFRT total score (P < 0.01) were significantly different between the groups. TUGT results were 7.79 ± 1.54 s and 10.13 ± 2.63 s, respectively, in group 1 and 2 (z = −2950; P < 0.01). No statistically significant difference between groups in any performance parameters of the 6MWT was found (P ≥ 0.05). Anterior body balance was found to be dominant in group 1, while posterior body balance was dominant in group 2 (P ≤ 0.05) measured by stabilometric platform. Conclusions: The distal group was particularly affected regarding dynamic balance, and the proximal group regarding static balance. Muscle strength was important for providing dynamic stability in the distal group, and for maintaining proximal stabilization during dynamic activities in the proximal group.
Key words balance, Duchenne muscular dystrophy, muscle weakness, neuropathy.
Neuromuscular disease (NMD) is a hereditary or acquired disorder of the peripheral neuromuscular system affecting anterior horn motor neurons, peripheral nerves, neuromuscular junction and muscles.1 Neuromuscular disorders are subclassified according to the location of the lesion within the peripheral neuromuscular system.2 When anatomic location is considered as a basis for classification, commonly encountered neuromuscular disorders are muscle disorders, motor neuron disorders and neuromuscular junction disorders.3,4 Muscle weakness and hypotonia is the common characteristics of neuromuscular disorders in infancy and childhood. Distribution of muscle weakness and related neurological findings (especially, changes in deep tendon reflexes or sensory loss) usually indicate the primary affected area within the neuromuscular system.4 The pathology in one of the most Correspondence: ˙Ipek Alemdarog˘lu, PT PhD, Physiotherapy and Rehabilitation Department, Faculty of Health Sciences, Bezmialem Vakıf University, 34100, Fatih, Istanbul/Turkey. Email: [email protected]
Received 10 March 2014; revised 7 May 2014; accepted 4 June 2014.
© 2014 Japan Pediatric Society
common NMD, Duchenne muscular dystrophy (DMD), which is characterized by proximal muscle involvement of the limbs, is caused by lack of dystrophin, which is a protein component of the glycoprotein complex within the muscle fiber sarcolemma. In another common childhood hereditary disease, Charcot-MarieTooth (CMT), which is characterized primarily by involvement of distal muscles and is also termed ‘hereditary motor-sensory neuropathy’ (HMSN), there is pathology of the motor and sensory fibers of the peripheral nerves.4 It has been reported that loss of balance, which is a commonly encountered symptom in NMD, is usually caused by loss of muscle strength (proximal, distal or both).5–7 The importance of muscle weakness in patients with NMD is twofold. First, distal leg weakness has a tendency toward instability disorders such as stumbling, but it has been observed that proximal muscle weakness lowers stability following external balance perturbations.7 Second, in the Horlings et al. study, it was found that compensatory strategies for maintaining balance differ in patients with NMD with distal or proximal muscle weakness depending on the localization of muscle weakness. In that study, depending on the localization of muscle weakness, there was more instability in patients with distal involvement compared to proximal weakness.
Muscle weakness and balance in NMD Also, in patients with distal involvement, severity of muscle weakness had a more profound effect over instability.8 In the literature, the number of articles on the separate effects of proximal and distal muscle weakness on function, and on the functional differences arising from the two different weakness patterns, is limited.7,8 The aims of the present study were (i) to assess and compare the static and dynamic balance in NMD children with proximal and distal muscle weakness in the early stage of the disease; and (ii) to identify how static and dynamic balance, which differ due to muscle weakness distribution, are translated into functional capacity (performance).
Forty pediatric patients with a diagnosis of DMD, HMSN, motor neuropathy (MN) and polyneuropathy (PNP) were enrolled in the study after obtaining written informed consent from their parents and themselves. Ethics approval for the study was obtained from Hacettepe University, Non-invasive Clinical Researches Ethics Committee. The inclusion criteria were as follows: (i) age 6–18 years; (ii) no additional neurological disease; (iii) able to walk independently at least 10 m (with or without assisted walking devices); (iv) able to cooperate with the instructions of the evaluator; (v) no orthopedic disorder of the lower limbs preventing application of assessment batteries within the last 6 months; and (vi) no cardiopulmonary disorder preventing application of performance tests. Subjects with mental retardation or who were uncooperative with the instructions of the evaluator, or who had any other chronic disease unrelated to their own disease, and were not able to walk independently at least 10 m, were excluded from the study. Functional level was assessed using the Brooke lower extremity functional classification (BLEFC), developed in 1981.9 According to this classification, children are classified between grade 1 (walks and climbs stairs without assistance) and grade 10 (confined to bed). Children in grade 1, 2 or 3 (those still ambulatory) were included in the study. Procedure
The children included into the study were separated into groups according to diagnosis. Twenty children diagnosed with DMD with primarily proximal muscle involvement were assigned to group 1, and 20 children diagnosed with HMSN, MN or PNP with primarily distal muscle involvement were assigned to group 2. Demographic data including age (years), height (cm), weight (kg) and body mass index (kg/cm2) were recorded, and then the following assessments were performed in both groups.
areas was measured, and total and region muscle strength scores were recorded. Muscle strength scores obtained from right and left limbs were classified as ankle, knee, hip, neck and trunk, shoulder, elbow, and wrist regions. Regional muscle strength was calculated by adding muscle strength scores of individual muscles in each region, and the addition of regional muscle strength scores of lower and upper limbs provided lower limb, upper limb and trunk muscle strength scores. Addition of muscle strength scores for each region was done as follows: • neck and trunk region score from neck flexor, extensor, torso flexor and extensor muscles; • hip region score from hip flexor, extensor, abductor, adductor, internal and external rotator muscles; • knee region score from knee flexor and extensor muscles; • ankle region score from dorsi and plantar flexor, invertor and evertor muscles; • shoulder region score from serratus anterior, trapezius uppermiddle-lower, deltoid anterior-mid-posterior and shoulder extensor muscles; • elbow region score from elbow flexor and extensor, forearm supinator and pronator muscles; • wrist region score from wrist flexor and extensor muscles. Total muscle strength score is obtained as the total of all regions of the right and left limb. Balance assessment
Static and dynamic balance were assessed using the (i) pediatric functional reach test (PFRT); (ii) timed up-and-go test (TUGT); and (iii) Stabilometric platform. Pediatric functional reach test
This test, which is used for assessing static balance, is a reliable and valid modified form of the Function Research Test.12,13 It includes subsections for side (left and right) and for forward reaching in the sitting and standing positions.12,13 Subsections of the test are as follows: (i) sitting in a chair (without back support): if the child can sit for 15 s independently, and (a) reach forward, (b) reach to the right, (c) reach to the left in the sitting position; and (ii) standing: if the child can stand independently for 15 s, and (d) reach forward, (e) reach to the right, and (f) reach to the left in the standing position. The children were asked to lift their arms 90° forward and to the sides (right and left) and reach as far as possible while sitting and standing. Reaching distance was measured in centimeters in each subsection by marking the end point of the third finger over a rule marked on a wall and recorded as “baseline”, “final” and “difference”; the total score was obtained by adding the “difference” of all subsections.
Assessment of muscle strength
The strength of 30 muscle groups in the lower limbs, trunk and upper limbs was assessed using Dr. Lovett’s manual muscle test.10,11 In this method muscle strength is graded between 0 (full paralysis) and 5 (normal). Muscle strength of the predetermined
Timed up-and-go test
The aim of this test, which assesses dynamic balance, is to evaluate balance performance during mobility. It has been shown to be a valid and reliable method of assessing dynamic balance.14 © 2014 Japan Pediatric Society
P Kaya et al.
The children were asked to stand up from their chair and walk 3 m at their usual speed and return and sit down on the chair again. The duration was measured by a chronometer and recorded in seconds. An average of three assessments done consecutively after a time for rest was considered as the final result of the test. Stabilometric platform
For the assessment of gravitational deviation the PaganiTM Stabilometric platform (Elettronica Pagani, Italy) was used. Stabilometric platform is a non-invasive method of measuring swing of the body during the standing position. This system consists of a 50 × 50 cm platform monitoring bodyweight and position of the gravity center continuously, and a computer system attached to the platform. Children were asked to stand on the platform with an angle between the feet of 30° and distance between the heels of 2 cm in a comfortable but erect position, looking forward and to count silently. Assessment time was determined with eyes open (30 s) and eyes shut (30 s) for a total of 60 s. During the assessment audiovisual stimulus that would distract the child was avoided.15 At the end of the stabilometric assessment, the average of the anterior–posterior movements of the gravity center and the average of mediolateral movements of the gravity center were recorded in millimeters. Body balance was calculated by the stabilometric device automatically as percent (%) for anterior/ posterior balance and right/left balance, defining deviation as that from the reference points of the gravity line on body segments. Assessment of functional capacity
The 6 min walk test (6MWT) is an important primary outcome measure that has been used in recent years in clinical studies, especially in DMD patients.16 6MWT is a frequently used method to evaluate functional capacity and endurance in activities of daily living (ADL) and has been proved to be valid in pediatric patients.17,18 In the present study, functional capacity was evaluated with 6MWT using the method recommended by the American Thoracic Society, which is modified for pediatric patients.17 The 6MWT was performed indoors, in a flat, linear, enclosed corridor with a hard floor of eight steps’ width. The test field was marked out by tape for a length of 25 m. Arrows were placed on the floor with tape to indicate movement in an anticlockwise direction. One cone each was placed at the beginning and at the end of the test distance. The children were asked to walk as fast as they could without running or jumping. The 6 min walk distance (6MWD) was measured in meters (m) with a measuring tape; and the number of completed circuits, and steps, walking speed (m/s) and cadence (no. steps/min) were recorded.16–21
Table 1 Physical features
Age (years) Height (cm) Weight (kg) BMI (kg/cm2)
comparison of continuous variables with normal distribution, and Mann–Whitney U-test for intergroup comparison of variables with non-normal distribution. Statistical significance was set at 0.05.
Results Of the 40 pediatric patients, 20 (50%) were diagnosed with DMD, 13 (32.5%) with HMSN, five (12.5%) with MN, and two (5%) with PNP according to genetic analysis and electromyography as well as clinical symptoms. Physical characteristics of group 1 (DMD) and group 2 (HMSN, MN, PNP) are listed in Table 1. BLEFC distribution is given in Table 2. Muscle strength
The muscle strengths of hip, around-knee, total lower limbs, shoulder, around-elbow, total upper limbs and trunk muscles were found to be statistically different between group 1 and group 2 (P < 0.05; Table 3). Balance
There were statistically significant differences between the two groups in the forward and right side reach subsections in the sitting position, and total score of PFRT (P < 0.01; Table 4). The TUGT was completed in 7.79 ± 1.54 s in group 1 and in 10.13 ± 2.63 s in group 2. TUGT results were found to be statistically significant between groups (z = −2950; P < 0.01). Static balance assessment using stabilometry showed that there was no difference between groups regarding anteroposterior and mediolateral movements of the gravity center and lateral balance to the right and left (P > 0.05), but there was a statistically significant difference between the groups in anterior and posterior body balance (P < 0.05). Stabilometric platform results are listed in Table 5.
Table 2 BLEFC distribution BLEFC
© 2014 Japan Pediatric Society
Group 2 (n = 20) (Mean ± SD) 12.95 ± 3.3 147 ± 19.16 38.02 ± 11.65 17.42 ± 3.81
BMI, body mass index.
SPSS 13.0 was used for statistical analysis.22,23 Categorical variables are described as frequency and percentage, and continuous variables as mean ± SD. The fit of continuous variables to normal distribution was tested with Shapiro–Wilk test. Significance of the difference between two means test was used for intergroup
Group 1 (n = 20) (Mean ± SD) 9.05 ± 3.1 122.85 ± 7.67 28.5 ± 4.93 18.91 ± 3.1
Grade 1 Grade 2 Grade 3 Total
Group 1 (n = 20)
Group 2 (n = 20)
n 10 7 3 20
n 14 5 1 20
% 50 35 15 100
BLEFC, Brooke lower extremity functional classification.
% 70 25 5 100
Muscle weakness and balance in NMD
Table 3 Muscle strength Parameters of muscle strength Lower extremity muscle strength Around hip (0–60) Around knee (0–20) Around ankle (0–40) Lower extremity total (0–120) Upper extremity muscle strength Around shoulder (0–80) Around elbow (0–40) Around wrist (0–20) Upper extremity total (0–140) Neck and Trunk Muscle Strength (0–40)
Group 1 (n = 20) (Mean ± SD)
Group 2 (n = 20) (Mean ± SD)
34.15 ± 10.12 15.3 ± 3.32 33.7 ± 6.24 81.5 ± 18.75
48.84 ± 8.48 17.85 ± 2.18 31.05 ± 8.49 98.7 ± 16.59
−3.873 −2.459 −0.462 −2.764
0.00** 0.01* 0.66 0.00**
65.25 ± 11.95 31.7 ± 6.5 16.6 ± 2.85 113.8 ± 18.38 15.15 ± 2.71
77.65 ± 10.25 37.45 ± 2.85 17.45 ± 3.17 132.55 ± 13.99 17.55 ± 1.9
−3.033 −2.851 −1.005 −3.086 −2.786
0.00** 0.00** 0.34 0.00** 0.00**
*P < 0.05; **P < 0.01.
There was no statistically significant difference between groups in any performance parameters of the 6MWT (P > 0.05; Table 6).
Discussion The main objective of the present study was to assess balance and functional capacity difference between NMD patient groups having primarily proximal or distal muscle weakness. In the first group with proximal muscle weakness hip, around-knee, total lower limb, shoulder, around-elbow and total upper limb muscle strength scores were found to be lower than in the second group with distal muscle weakness. Children with involvement of proximal muscle completed the dynamic balance test (TUGT)
more quickly, but in the static balance assessment (PFRT) children with distal muscle involvement scored higher in forward and right side reach parameters and the total score. Additionally; anterior balance was found to be dominant in patients with proximal muscle involvement, while posterior balance was dominant in patients with distal muscle involvement. The performance in children grouped according to distribution of muscle weakness was not affected by changes in balance parameters. There is a limited number of studies in the literature on the effect of diseases with proximal and distal involvement on performance, but they all assessed distal or proximal involvement separately. There are studies investigating effects of muscle weakness distribution on function and balance.7,8 In similar studies, it has been shown that muscle weakness distribution has
Table 4 PFRT scores PFRT subsection Sitting Forward reach distance (cm) Right side reach distance (cm) Left side reach distance (cm) Standing Forward reach distance (cm) Right side reach distance (cm) Left side reach distance (cm) Total score
Group 1 (n = 20) (Mean ± SD)
Group 2 (n = 20) (Mean ± SD)
23.27 ± 6.02 16.90 ± 4.56 19.55 ± 5.78
33.70 ± 7.44 22 ± 4.47 23.1 ± 3.94
−3.999 −3.460 −1.603
0.00** 0.00** 0.11
21.40 ± 5.55 17.05 ± 3.17 19.2 ± 3.73 117.37 ± 15.68
20.8 ± 7.66 17.4 ± 3.06 20.62 ± 7.16 137.57 ± 19.83
−0.298 −0.424 −1.045 −2.896
0.78 0.68 0.30 0.00**
**P < 0.01. PFRT, pediatric functional reach test. Table 5 Stabilometer swing results Stabilometer parameters Antero-posterior swing (mm) Mediolateral swing (mm) Anterior balance (%) Posterior balance (%) Right lateral balance (%) Left lateral balance (%)
Group 1 (Mean ± SD) 11 ± 14.16 21 ± 25.5 53.95 ± 5.55 47.5 ± 5.2 48.4 ± 2.86 51.5 ± 3.01
Group 2 (Mean ± SD) 15.5 ± 14.63 44 ± 28.72 57.5 ± 4.72 43.15 ± 5.25 49.3 ± 2.89 49.7 ± 4.44
−0.244 −1.665 −2.002 −2.097 −1.042 −1.678
0.82 0.10 0.05* 0.04* 0.30 0.10
*P ≤ 0.05.
© 2014 Japan Pediatric Society
P Kaya et al.
Table 6 6MWT results 6MWT parameters No. completed circuits in 6 min Total distance covered in 6 min (m) Walking velocity in 6 min (m/s) Total no. steps in 6 min Cadence (no. steps/min)
Group 1 (Mean ± SD) 17.30 ± 3.85 349.70 ± 77.18 58.77 ± 12.53 735.65 ± 102.95 122.60 ± 16.27
Group 2 (Mean ± SD) 17.97 ± 3.8 358.85 ± 75.07 59.8 ± 12.51 664.85 ± 115.49 110.80 ± 19.24
−0.582 −0.609 −0.446 −1.718 −1.718
0.57 0.55 0.66 0.09 0.09
6MWT, 6 min walk test.
an effect on function and balance.24,25 There is a lack, however, of comparative studies investigating effects of the two separate weakness patterns on balance and function in patients with NMD who are grouped according to region of muscle weakness. Detailed pathophysiological studies investigating underlying mechanisms of postural instability in patients with NMD are also limited. Given that different NMD involve different specific muscle weakness patterns, specific studies on balance control mechanisms are needed. Owing to the limited number of studies assessing how specific muscle weakness patterns affect balance, it has been difficult to develop effective fall prevention strategies for these patients.7,8 The peripheral nervous system component of the efferent postural control system is under-evaluated in previous studies. A healthy muscle system is important for balance control, because a fundamental effector in producing balance reactions and sustaining postural control requires proper musculoskeletal system function along with an intact central nervous system.7 The importance of muscle strength in preserving balance was emphasized in a study that investigated the effects of muscle weakness region on balance.8 Baret et al. found a linear but insignificant correlation between position of gravity center and total muscle strength and walk time in patients with DMD.26 In the present study, we found that static balance was more negatively affected in DMD patients with proximal muscle involvement compared to patients with neuropathy because of muscle weakness distribution, but dynamic balance was better. This finding suggests that proximal muscle involvement affects static balance from the very beginning of the disease in patients with proximal muscle involvement. In other words, in the group with proximal muscle involvement, the first effects of the loss of balance due to postural adaptation developing as a result of affected antigravity muscles, are observed on static balance. In the present study, dynamic balance was affected in the group with distal muscle involvement. This may be because of two reasons. First, the affected muscle group plays an essential role in dynamic functions, and it is located in the distal regions of the body; second, postural compensation mechanisms may be observed in the later stages of the disease, as the weakness of the antigravity muscles, which play a fundamental role in static balance, reaches a certain level. In order to carry out most of the functional ADL, postural control must be preserved and thus preservation of both dynamic and static balance is needed. The TUGT and PFRT are reliable and valid methods for the assessment of balance in pediatric patients,27 but use of these methods in patients with NMD is limited. © 2014 Japan Pediatric Society
When used as a measure of disability in physically disabled patients, TUGT allows identification of functional mobility and dynamic balance alterations in the clinic, and facilitates probable future therapeutic intervention by allowing observation of gait, speed in transfers and turning activities, which may highlight the physical disorder that must be elaborated.28 In a study investigating the validity and reliability of TUGT in pediatric subjects, the mean TUGT score in 176 healthy children with a mean age of 5.9 ± 1.8 years was 5.9 ± 1.3 s; in 501 Indonesian children between 4 and 9 years old it was 6.1 s. It has been reported that TUGT is a reliable method of assessing dynamic balance in 3–9-year-old children.28 Mean TUGT in four spastic hemiplegic children 8.11 ± 4.3 years of age was 8.4 ± 1.3 s, in 22 spastic quadriplegic children it was 10.1 ± 2.4 s and in six spastic diplegic children it was 28.0 ± 26.0 s, and in seven children with myelomeningocele it was 8.0 ± 1.5 s.28 Gan et al. measured TUGT score as 25.9 ± 30.4 s in 30 children with different types of cerebral palsy who were between 60 and 142 months old.29 Accordingly, it has been reported that TUGT is a valid method that can be used in 3–19-year-old physically disabled children.28 In the present study, children in both groups completed TUGT in a longer period of time than their healthy peers. This was interpreted as an indicator of insufficient dynamic balance in both groups regardless of muscle weakness distribution. Completion of the test in a longer time in the distal group compared to the proximal group suggests that among patients with neuromuscular disorders, dynamic stability was affected in children with distal weakness more than in those with proximal weakness, even though these different muscle weakness patterns occur at the same functional level. In the present proximal group, the PFRT results for forward reach, right side reach and total score parameters in the sitting position were lower. In the PFRT, in the presence of a stable support surface, forward mobility puts strain on the forward limit of stability. During this activity, the greatest lower limb joint movement occurs in hip joints. In order to control this movement, the posterior muscles of the hip and trunk should contract eccentric to control the movement, and anterior muscles should contract concentric to perform the movement. With this in mind, during this test, around-hip and trunk muscle strength is important in order to sustain stability. This suggests that exercise programs targeting increase and preservation of hip and trunk muscle strength are needed to facilitate performance of dynamic ADL that require reaching. Weakening specifically of these muscles in the proximal group (according to the region of muscle weakness) may be considered as the most important disadvantage
Muscle weakness and balance in NMD of this group. It should be considered, however, that, also in the distal group, particular exercise of proximal and trunk muscles starting from the early period of treatment programs, may be helpful in preserving/increasing performance. In the present study, in the two groups of NMD patients with different muscle weakness distribution, the 6MWD, number of completed circuits, walking speed, number of total steps and cadence were similar. The lack of alteration in walking, which is one of the fundamental ADL, combined with the presence of changes in static and dynamic balance in both NMD groups with different muscle weakness distribution, was probably because the children were in an earlier phase of their disease. The present results also indicate, in the proximal group, despite loss of balance of differing severity, functional performance may still be preserved until the loss of muscle strength becomes more obvious. In a similar manner, walking performance may be directly affected by the increasing severity of loss of balance in the distally affected group because of the disease characteristics at later time. Using the TUGT and PFRT, the importance of muscle strength in providing dynamic stability in the distal group and in maintaining proximal stabilization during dynamic activities in the proximal group, has been demonstrated. The distal group was particularly affected in dynamic balance compared to the proximal group, and the proximal group in static balance compared to the distal group. Consideration of the identified differences in balance parameters within the distal and proximal groups during the course of the disease, in the planning and implementation of therapeutic approaches, is the key to increase the success of physiotherapy and rehabilitation programs. Limitations
Lack of assessment of superficial and deep sensory responses in neuropathic patients with primarily distal muscle involvement was a limitation of the present study. Further studies are needed in neuropathic patients in order to assess the effects of sensory loss on performance of activities of daily living.
Acknowledgment There is no conflict of interest and no specific funding for this study.
References 1 McDonald CM. Physical activity, health impairments, and disability in neuromuscular disease. Am. J. Phys. Med. Rehabil. 2002; 81: 108–20. 2 Özsarlak Ö, Schepens E, Parizel PM et al. Hereditary neuromuscular diseases. Eur. J. Radiol. 2001; 40: 184–97. 3 Andersson PB, Rando TA. Neuromuscular disorders of childhood. Curr. Opin. Pediatr. 1999; 11: 497–503. 4 Dubowitz V. Muscle Disorders in Childhood. WB Saunders, Philadelphia, 1995. 5 Moreland JD, Richardson JA, Goldsmith CH, Clase CM. Muscle weakness and falls in older adults: A systematic review and metaanalysis. J. Am. Geriatr. Soc. 2004; 52: 1121–9. 6 Pieterse AJ, Luttikhold TB, de Laat K, Bloem BR, van Engelen BG, Munneke M. Falls in patients with neuromuscular disorders. J. Neurol. Sci. 2006; 251: 87–90.
7 Horlings CG, van Engelen BG, Allum JH, Bloem BR. A weak balance: The contribution of muscle weakness to postural instability and falls. Nat. Clin. Pract. Neurol. 2008; 4: 504–15. 8 Horlings CG, Küng UM, van Engelen BG et al. Balance control in patients with distal versus proximal muscle weakness. J. Neurosci. 2009; 164: 1876–86. 9 Brooke MH, Griggs RC, Mendell JR, Fenichel GM, Shumate JB, Pellegrino RJ. Clinical trial in Duchenne dystrophy: The design of the protocol. Muscle Nerve 1981; 4: 186–97. 10 Saadet O, Demirel H, Sade A. Tedavi Hareketlerinde Temel Deg˘erlendirme Prensipleri. HÜ Fizik Tedavi ve Rehabilitasyon Yüksekokulu Yayınları, Ankara, 2003 (in Turkish). 11 Aras Ö. DMD’li çocuklarda kas kuvveti deg˘erlendirmelerinin kars¸ılas¸tırılması. Hacettepe University Master of Science Thesis, Ankara, 1997 (in Turkish). 12 Bartlett D, Birmingham T. Validity and reliability of a pediatric reach test. Pediatr. Phys. Ther. 2003; 15: 84–92. 13 Duncan PW, Weiner DK, Chandler J, Studenski S. Functional reach: A new clinical measure of balance. J. Gerontol. 1990; 45: 192–7. 14 Wall JC, Bell C, Campbell S, Davis J. The Timed Get-up-and-Go test revisited: Measurement of the component tasks. J. Rehabil. Res. Dev. 2000; 37: 109–13. 15 Elettronica Pagani. Posturology and Satabilometry mod: Postural Equa 2, Class II, Type BF. Paderno, Italy. [Cited 7 July 2014.] Available from URL: http://www.elettronicapagani.com, 2003. 16 McDonald CM, Henricson EK, Han JJ et al. The 6-minute walk test as a new outcome measure in Duchenne muscular dystrophy. Muscle Nerve 2010; 25: 500–10. 17 ATS statement: guidelines for the six minute walk test. Am. J. Respir. Crit. Care Med. 2002; 166: 111–17. 18 Lammers AE, Hislop AA, Flynn Y et al. The 6-minute walk test: Normal values for children of 4–11 years of age. Arch. Dis. Child. 2008; 93: 464–8. 19 Li AM, Yin J, Au JT et al. Standard reference for the six-minutewalk test in healthy children aged 7 to 16 years. Am. J. Respir. Crit. Care Med. 2007; 176: 174–80. 20 Geiger R, Strasak A, Treml B et al. Six-minute walk test in children and adolescents. J. Pediatr. 2007; 150: 395–9. 21 Li AM, Yin J, Yu CC et al. The six-minute walk test in healthy children: Reliability and validity. Eur. Respir. 2005; 25: 1057–60. 22 Predictive Analytics Software and Solutions. SPSS Software, [Cited 7 July 2014.] Available from URL: http://www.spss.com, 2014. 23 SPSS 13.0 Brief Guide. SPSS Software, [Cited 7 July 2014.] Available from URL: http://brain.mcmaster.ca/SPSS.manual/ SPSS%20Brief%20Guide%2013.0.pdf, 2014. 24 Saguil A. Evaluation of the patient with muscle weakness. Am. Fam. Physician 2005; 71: 1327–36. 25 Berthelsen MP, Husu E, Christensen SB, Prahm KP, Vissing J, Jensen BR. Anti-gravity training improves walking capacity and postural balance in patients with muscular dystrophy. Neuromuscul. Disord. 2014; 24: 492–8. 26 Barrett R, Hyde SA, Scott OM, Dubowitz V. Changes in center of gravity in boys with Duchenne muscular dystrophy. Muscle Nerve 1988; 11: 1157–63. 27 Westcott SL, Lowes LP, Richardson PK. Evaluation of postural stability in children: Current theories and assessment tools. Phys. Ther. 1997; 77: 629–45. 28 Williams EN, Carroll SG, Reddihough DS, Phillips BA, Galea MP. Investigation of the timed “up & go” test in children. Dev. Med. Child Neurol. 2005; 47: 518–24. 29 Gan SM, Tung LC, Tang YH, Wang CH. Psychometric properties of functional balance assessment in children with cerebral palsy. Neurorehabil. Neural Repair 2008; 22: 745–53.
© 2014 Japan Pediatric Society
Copyright of Pediatrics International is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.