Abstract
[Purpose] To investigate the effects of progressive functional training on lower limb muscle architecture and motor function of children with spastic cerebral palsy (CP). [Subjects] The subjects of this study were 26 children with spastic CP. [Methods] Thirteen subjects in the experimental group performed general neurodevelopmental treatment (NDT) and additional progressive functional trainings and 13 subjects in the control group performed only general NDT 3 times a week for 6 weeks. Ultrasonography, gross motor function measurement (GMFM) and the mobility questionnaire (MobQue) were evaluated. [Results] After the intervention, the muscle thickness of the quadriceps femoris (QF), cross-sectional area of the rectus femoris (RF), pennation angle of the gastrocnemius (GCM) and the MobQue score of the experimental group were significantly greater than those of the control group. The muscle thickness of QF correlated with the cross-sectional area (CSA) of RF and the pennation angle of GCM, and GMFM score correlated with the pennation angle of GCM. [Conclusion] Progressive functional training can increase muscle thickness, CSA, and the pennation angle of the lower limb muscles, and improve the mobility of spastic CP children making it useful as a practical adjunct to rehabilitation therapy.
Key words: Cerebral palsy, Function, Ultrasonography
INTRODUCTION
Cerebral palsy (CP) is not a progressive diseases, but movement problems and musculoskeletal disorders in CP may change over time1). In order to lessen the movement problems and musculoskeletal disorders of cerebral palsy, progressive functional training is used2,3,4). In a previous study, progressive functional training significantly improved muscle strength. However, walking ability and anaerobic muscle power did not change. In addition, spasticity and range of motion remained unchanged2). Thus, investigation of muscles architecture changes are required to assess cerebral palsy treatments.
Clinically, many measures of cerebral palsy are difficult to use in objective and quantitative analysis, because they are qualitative assessments of performance and dysfunction degree. Therefore, magnetic resonance imaging or ultrasound imaging are needed for the assessment of muscular architecture, e.g. muscle thickness, cross-sectional area, and pennation angle5, 6). So far, few studies have investigated the effectiveness of interventions using quantitative analysis of muscular architecture changes in CP. Therefore, the purpose of this study was to evaluate the effectiveness of the progressive functional training using ultrasonography of lower limb muscular architecture and motor function of spastic CP children.
SUBJECTS AND METHODS
We enrolled 26 spastic CP children. The inclusion criteria were an age between 5 and 10 years, the ability to follow verbal instructions, and the ability to walk independently indoors with or without walking aids (Gross Motor Function Classification; GMFCS levels I–III). The exclusion criteria were unstable seizures, any treatment for spasticity or surgical procedures in the 6 months before the study, any change in medication expected during the study period, of any other disease that would have interfered with physical activity.
This study lasted for 6 weeks and had a single-blind randomized controlled design. The purpose of the study was explained to the participants or caregivers, and their informed consent was obtained. The study protocol was approved by the institutional review board of Sahmyook University, Seoul.
The control group received 30 minutes general neurodevelopmental treatment (NDT), 3 sessions a week for 6 weeks. The experimental group received the same 30 minutes general NDT with an additional progressive functional training program, 3 sessions a week for 6 weeks. The progressive functional training program consisted of warm-up exercise using range of motion and stretching for 3 minutes, followed by three functional training items: loaded sit-to-stand for 5 minutes, loaded lateral step-up and half knee-rise for 10 minutes, and unloaded lateral step-up and half knee-rise for 10 minutes. To finish the program, a 2-minute cool-down exercise using a tension-relaxation was used. The training load was initially set to 5% of subjects’ body weights and progressively increased, based on repeated estimation of the eight-repetition maximum7). After performing each training item, a break of 1–2 minutes was provided.
Ultrasonography (US), gross motor function measurement (GMFM), and the mobility questionnaire (MobQue) were evaluated before and after the intervention. An ultrasonography system (Medison Myosone, U5, Samsung, Korea) with a 6–12-MHz, 2D B-mode linear transducer was used to obtain images of the quadriceps femoris (QF), rectus femoris (RF), and gastrocnemius (GCM). The right side muscle thickness of QF, cross-sectional area (CSA) of RF, and the muscle thickness and pennation angle of GCM were measured. The US measurements were carried out by one examiner who had 5 years experience in musculoskeletal US. The average values of three measures were calculated and used in the analysis.
In order to assess the motor function of subjects, the Gross Motor Function Measurement-88 (GMFM-88) was conducted by one pediatric physical therapist who had 3 years of experience in GMFM-88. Subjectively reported mobility was assessed with the MobQue which consists of 47 questions assessing caregiver-reported mobility limitations.
SPSS ver. 18.0 statistical software was used for statistical analyses. The Kolmogorov-Smirnov test was used to examine the normality of the data, which were found to be normally distributed. The χ2 test and independent t-test were used to assess the homogeneity of the groups. The paired t test was used to test the significance of differences in the pre- and post-intervention values of each group. The independent t-test was implemented to test the significance of differences between the control and experimental groups after the intervention. Finally, the Pearson correlation coefficient was used to investigate the relationships between each muscles’ architecture items and motor function in the two groups. Significance was accepted at p < 0.05.
RESULTS
The general characteristics of both groups are shown in Table 1. After the intervention, the thickness of QF, CSA of RF, and the pennation angle of GCM showed significant increases in the experimental group (p<0.05) (Table 2). The MobQue score of the progressive functional training group showed a significant improvement compared to the control group (p<0.05). The GMFM score of the experimental group increased more than that of the control group, but was not significantly different (Table 3). Pearson correlation coefficients show that the thickness of QF correlated with the CSA of RF and the pennation angle of GCM (r=0.763, r=0.452, p<0.01, p<0.05); CSA of RF correlated with the GCM thickness and pennation angle (r=0.519, r=0.537, p<0.01); and the thickness of GCM correlated with the pennation angle of GCM (r=0.521, p<0.01). In addition, the GMFM score correlated with the pennation angle of GCM (r=0.585, p<0.01) (Table 4).
Table 1. The general characteristics of the subjects.
| Parameters | Groups | |
|---|---|---|
| Experimental group (n=13) |
Control group (n=13) |
|
| Gender | ||
| Male/Female (%) | 8/5 (61.5/38.5) | 5/8 (38.5/61.5) |
| Age, years | 6.1 (2.7) | 6.9 (2.5) |
| Height, cm | 107.2 (21.8) | 118.0 (27.6) |
| Weight, kg | 19.1 (8.2) | 25.8 (16.4) |
| BMI, kg/m2 | 16.3 (1.9) | 17.1 (3.6) |
Values are n (%) or mean (SD), There was no significant differences between the groups. BMI: body mass index
Table 2. Comparison of muscle architecture of the lower limb between groups, and before and after intervention.
| Parameter | Groups | ||
|---|---|---|---|
| Experimental group (n=13) |
Control group (n=13) |
||
| QF thickness (cm) | Pre | 1.6 (0.2) | 1.8 (0.2) |
| Post | 1.9 (0.2)** | 1.7 (0.3) | |
| Change | 0.3 (0.2)** | −0.1 (0.3) | |
| RF CSA (cm2) | Pre | 1.2 (0.5) | 1.7 (0.6) |
| Post | 2.1 (0.7)** | 1.6 (0.5) | |
| Change | 0.9 (0.7)** | −0.1 (0.7) | |
| GCM thickness (cm) | Pre | 0.7 (0.1) | 0.8 (0.2) |
| Post | 1.0 (0.1)** | 1.0 (0.2) | |
| Change | 0.3 (0.2) | 0.2 (0.4) | |
| GCM pennation angle (o) | Pre | 14.9 (6.2) | 17.8 (8.2) |
| Post | 17.9 (3.5)* | 15.6 (3.4) | |
| Change | 3.0 (4.6)* | −2.2 (6.4) | |
Values are mean (SD); *indicates significant difference, p<0.05; **indicates significant difference, p<0.01. QF: Quadriceps femoris; RF: rectus femoris; CSA: cross-sectional area; GCM: gastrocnemius
Table 3. Comparison of GMFM and MobQue scores between groups and before and after intervention.
| Parameter | Groups | ||
|---|---|---|---|
| Experimental group (n=13) | Control group (n=13) | ||
| GMFM (score) | Pre | 78.0 (19.1) | 79.1 (14.7) |
| Post | 81.9 (16.1)** | 81.3 (14.3)** | |
| Change | 3.9 (4.0) | 2.1 (1.9) | |
| MobQue (score) | Pre | 55.7 (29.9) | 48.3 (26.9) |
| Post | 66.9 (26.7)** | 51.5 (25.7) | |
| Change | 11.2 (8.8)* | 3.2 (10.6) | |
Values are mean (SD); *indicates significant difference, p<0.05; **indicates significant difference, p<0.01. GMFM: Gross Motor Function Measurement; MobQue: Mobility Questionnaire
Table 4. Pearson correlation coefficient among muscle architectures and mobility function.
| Parameter | QF thickness (cm) |
RF CSA (cm2) |
GCM thickness (cm) |
GCM pennation angle (o) |
GMFM (score) |
MobQue (score) |
|---|---|---|---|---|---|---|
| QF thickness (cm) | 1 | |||||
| RF CSA (cm2) | 0.763** | 1 | ||||
| GCM thickness (cm) | 0.383 | 0.519** | 1 | |||
| GCM pennation angle (o) | 0.452* | 0.537** | 0.521** | 1 | ||
| GMFM (score) | 0.076 | 0.188 | 0.361 | 0.585** | 1 | |
| MobQue (score) | 0.112 | 0.175 | −0.093 | 0.136 | 0.112 | 1 |
Values are r (Pearson’s coefficient), *indicates significant correlation at p<0.05, **indicates significant correlation at p<0.01. QF: quadriceps femoris; RF: rectus femoris; CSA: cross sectional area; GCM: gastrocnemius; GMFM: Gross Motor Function Measurement; MobQue: Mobility Questionnaire
DISCUSSION
Progressive strength training can improve walking function and alignment as well as quality of life (QOL) of CP children8, 9). In addition, progressive functional strengthening may improve mobility functions such as walking speed, wheel chair propulsion, and sit-to-stand function10,11,12). Therefore, we investigated the mobility function of CP children with the MobQue before and after the intervention. The result of the MobQue analysis showed there was a significant increase in the score of the progressive functional training group. Additionally, the GMFM score showed a tendency to increase more in the experimental group than in the control group, but the result was not statistically significant. These results describe the effect of the progressive functional training which provides repeated functional practice with a load for the individual CP child.
Muscle weakness and motor disorder of spastic CP children are related to their functional level and their skeletal muscle architecture can dominate their muscle functions13). In order to measure the muscle architecture, we used ultrasonography. Ultrasonography can provide a quantitative measure of change in muscles, which correlate with muscle power and function14). Ultrasonography identified significant differences in CSA of RF, muscle thickness of QF, and the pennation angle and muscle thickness of GCM. In a previous study, muscle thickness of QF and GCM significantly increased with functional level15). The function of CP children significantly correlates with the muscle thickness of their vastus lateralis. And their mobility and transfer function abilities significantly correlate with the pennation angle of their vastus lateralis16).
In our study of muscle architectures, the thickness of QF, CSA of RF, and the pennation angle of GCM significantly increased after the intervention in the experimental group. In the correlation coefficient analysis, the GMFM score significantly correlated with the muscle thicknesses of QF and GCM, and the pennation angle of GCM.
Muscle weakness and changes in muscle architecture have long been recognized as primary clinical features of CP16). Our results show that the progressive functional training improved the muscle architecture items of muscle thickness, CSA, and the pennation angles of CP children who had pathological problems with their muscle function. These fine structural muscle changes may lead to improvement in function.
The findings of this study demonstrate that progressive functional training can increase muscle thickness, cross-sectional area, and the pennation angles of lower limb muscles, and improve the mobility of spastic CP, and can be used as a practical adjunct to rehabilitation therapy. A limitation of this study was that we could not divide the CP subjects into hemiplegia and diplegia groups due to the small number of subjects. We suggest further study implementing various individual treatments and using measurements of muscle architecture.
REFERENCES
- 1.Knox V, Evans AL: Evaluation of the functional effects of a course of Bobath therapy in children with cerebral palsy: a preliminary study. Dev Med Child Neurol, 2002, 44: 447–460. [DOI] [PubMed] [Google Scholar]
- 2.Scholtes VA, Becher JG, Janssen-Potten YJ, et al. : Effectiveness of functional progressive resistance exercise training on walking ability in children with cerebral palsy: a randomized controlled trial. Res Dev Disabil, 2012, 33: 181–188. [DOI] [PubMed] [Google Scholar]
- 3.Taylor NF, Dodd KJ, Baker RJ, et al. : Progressive resistance training and mobility-related function in young people with cerebral palsy: a randomized controlled trial. Dev Med Child Neurol, 2013, 55: 806–812. [DOI] [PubMed] [Google Scholar]
- 4.Boyd RN: Functional progressive resistance training improves muscle strength but not walking ability in children with cerebral palsy. J Physiother, 2012, 58: 197. [DOI] [PubMed] [Google Scholar]
- 5.Bilodeau M, Schindler-Ivens S, Williams DM, et al. : EMG frequency content changes with increasing force and during fatigue in the quadriceps femoris muscle of men and women. J Electromyogr Kinesiol, 2003, 13: 83–92. [DOI] [PubMed] [Google Scholar]
- 6.Maurits NM, Beenakker EA, van Schaik DE, et al. : Muscle ultrasound in children: normal values and application to neuromuscular disorders. Ultrasound Med Biol, 2004, 30: 1017–1027. [DOI] [PubMed] [Google Scholar]
- 7.VandenBerg NL: The use of a weighted vest to increase on-task behavior in children with attention difficulties. Am J Occup Ther, 2001, 55: 621–628. [DOI] [PubMed] [Google Scholar]
- 8.Damiano DL, Arnold AS, Steele KM, et al. : Can strength training predictably improve gait kinematics? A pilot study on the effects of hip and knee extensor strengthening on lower-extremity alignment in cerebral palsy. Phys Ther, 2010, 90: 269–279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Ko J, Lee BH, Kim M: Relationship between function and health-related quality of life of school-aged children with cerebral palsy. J Phys Ther Sci, 2011, 23: 189–195. [Google Scholar]
- 10.Latham NK, Bennett DA, Stretton CM, et al. : Systematic review of progressive resistance strength training in older adults. J Gerontol A Biol Sci Med Sci, 2004, 59: 48–61. [DOI] [PubMed] [Google Scholar]
- 11.Dodd KJ, Taylor NF, Damiano DL: A systematic review of the effectiveness of strength-training programs for people with cerebral palsy. Arch Phys Med Rehabil, 2002, 83: 1157–1164. [DOI] [PubMed] [Google Scholar]
- 12.Ko IH, Kim JH, Lee BH: Relationship between lower limb muscle structure and function in cerebral palsy. J Phys Ther Sci, 2014, 26: 63–66. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Damiano DL, Quinlivan J, Owen BF, et al. : Spasticity versus strength in cerebral palsy: relationships among involuntary resistance, voluntary torque, and motor function. Eur J Neurol, 2001, 8: 40–49. [DOI] [PubMed] [Google Scholar]
- 14.Chi-Fishman G, Hicks JE, Cintas HM, et al. : Ultrasound imaging distinguishes between normal and weak muscle. Arch Phys Med Rehabil, 2004, 85: 980–986. [DOI] [PubMed] [Google Scholar]
- 15.Ohata K, Tsuboyama T, Haruta T, et al. : Relation between muscle thickness, spasticity, and activity limitations in children and adolescents with cerebral palsy. Dev Med Child Neurol, 2008, 50: 152–156. [DOI] [PubMed] [Google Scholar]
- 16.Moreau NG, Teefey SA, Damiano DL: In vivo muscle architecture and size of the rectus femoris and vastus lateralis in children and adolescents with cerebral palsy. Dev Med Child Neurol, 2009, 51: 800–806. [DOI] [PMC free article] [PubMed] [Google Scholar]