Research in Developmental Disabilities 35 (2014) 2278–2283
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Research in Developmental Disabilities
Functional balance and gross motor function in children with cerebral palsy Silvia Leticia Pava˜o *, Kayo Andre F. Barbosa, Tatiana de Oliveira Sato, Nelci Adriana Cicuto Ferreira Rocha Department of Physiotherapy, Neuropediatrics Section, Federal University of Sa˜o Carlos, Rod. Washington Luis, km 235, 13565-905 Sa˜o Carlos-SP, Brazil
A R T I C L E I N F O
A B S T R A C T
Article history: Received 26 March 2014 Received in revised form 27 May 2014 Accepted 29 May 2014 Available online
Aims: To compare scores of children with cerebral palsy (CP) at different levels of Gross Motor Function Classification System (GMFCS), using the Pediatric Balance Scale (PBS) and to assess whether it can be used to predict GMFCS levels in children with CP. Methods: Fifty-eight children with CP levels I–V of GMFCS were assessed by PBS and grouped according to their GMFCS level. Results: It was observed differences in PBS scores between GMFCS I and II and between GMFCS II and III groups. Discriminant analysis indicated a 67% accuracy for the PBS instrument in assessing the GMFCS level of children with CP. Interpretation: PBS is able to detect differences among GMFCS levels I, II, and III of mild and moderate impairment. Accordingly, PBS can be used reliably in clinical practice to indicate the motor impairment level of such children. The results enable specify the expected tasks that are expected to be accomplished by the children in each GMFCS level, contributing with therapeutic planning and monitoring. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Cerebral palsy Pediatric Balance Scale GMFCS Postural control Scoring
1. Introduction Postural control demands the capacity to maintain center of mass within the limits of the support base and alignment of body segments (Castilho-Weinert & Forti-Bellani, 2011). Therefore, the performance of daily tasks such as self-care and mobility require postural control (Duarte & Freitas, 2010). Children with cerebral palsy (CP) besides presenting spasticity, muscular weakness, and adaptive modifications of muscle length (Assumpc¸a˜o, Piucco, Correˆa, & Ries, 2011), show a compromised capability to respond to loss of balance (Barela et al., 2011). Deficits in postural control in CP result from altered sensory processing and biomechanical alignment, which determine modified neuromuscular responses (Assumpc¸a˜o et al., 2011; Burtner, Qualls, & Woollacott, 1998; Woollacott et al., 1998). As these balance deficits impact the performance of daily activities (Ostensjo, Carlberg, & Vollestad, 2004), the assessment of postural control in children with CP is crucial to quantifying postural deficits, measuring rehabilitative progress, and also guide therapeutic interventions (Fig. 1). Several instruments have been validated for postural control evaluation including force plates (Ju, Hwang, & Cherng, 2012), electromyographic (Girolami, Shiratori, & Aruin, 2011) and joint angles analysis (Assumpc¸a˜o et al., 2011). The
* Corresponding author. Tel.: +55 16 3351 0467; fax: +55 16 3351 0467. E-mail address: [email protected] (S.L. Pava˜o). http://dx.doi.org/10.1016/j.ridd.2014.05.024 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
[(Fig._1)TD$IG]
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Fig. 1. Box plot of the total score of the Pediatric Balance Scale (PBS) among Gross Motor Function Classification System (GMFCS) groups.
complexity and cost of these instruments, however, significantly limit their use in clinical practice. Thus, the use of clinical scales such as the Pediatric Balance Scale (PBS) (Franjoine, Gunther, & Taylor, 2003; Reilly, Woollacott, van Donkelaar, & Saavedra, 2008) is simpler and may be a less expensive alternative to be used in clinical practice. PBS is a reliable instrument for assessment of functional balance in children with neuromotor impairments and assesses the elements of postural control that enable these children to perform daily activities effectively (Ries, Michaelsen, Soares, Monteiro, & Allegretti, 2012). Although PBS has been validated for use with such children (Franjoine et al., 2003; Ries et al., 2012) few studies have used it to evaluate balance in children with CP (Reilly et al., 2008) or have related PBS scores with GMFCS level in this population (Kembhavi, Darrah, Magill-Evans, & Loomis, 2002). Accordingly, the current study sought to evaluate the functional balance of children with CP using PBS, to identify differences in PBS total scores at distinct Gross Motor Function Classification System (GMFCS) levels, to set confidence intervals of PBS in each level of GMFCS and to assess whether PBS scores could be used as predictors of the GMFCS level in children with CP. Studying the differences in PBS total scores at distinct GMFCS levels, as well as assessing the PBS scores as predictors of the GMFCS level in children with CP will provide a broader understanding of balance abilities in each GMFCS level, specifying the expected tasks that are expected to be accomplished in each level. This approach will also facilitate the rehabilitation planning guiding some balance tasks to be accomplished by the children during physical therapy, as well as the measurement of clinical progress of the patients, since it can also predict the expected balance score the children must present according to their GMFCS level. 2. Methods 2.1. Participants The present study has a transversal design. Fifty-eight subjects (36 male, 22 female), with average age of 8.9 years (4.1), were selected at rehabilitation sites. All the included subjects were children with CP between 0 and 18 years old, and were involved in rehabilitation programs at least once a week. Written informed consent from the child’s legal guardian was also necessary. The study was authorized by the Ethics Committee for Research with Human Subjects of the Federal University of Sa˜o Carlos (protocol 363/2010). 2.2. Materials and procedure Children were classified according to GMFCS (Palisano et al., 1997) and divided into five groups according to their GMFCS level. GMFCS represents a functional classification of children with CP, which aims to determine the level of the child based
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on their abilities and limitations to perform gross motor function activities. Children can be classified according with five levels as follows: level I represents the ability to walk without limitations, level II indicates the ability to walk with limitations, level III is consisted of children that walk using a handheld mobility device; level IV includes children that present self-mobility with limitations, and level V is composed by children that are transported in a manual wheelchair (Palisano, Rosenbaum, Bartlett, & Livingston, 2008). Subjects’ functional balance was evaluated using the PBS (Franjoine et al., 2003). Derived from the Berg Balance Scale, which evaluates postural control in adults, PBS has been adapted and validated for the Brazilian population (Ries et al., 2012). PBS aggregate scores (hereafter PBS scores) for the 14 tasks evaluated can range from 0 to 56, with higher scores indicating better postural control. The evaluated tasks on PBS are the following: (1) sit to standing; (2) standing to sitting; (3) transfers; (4) standing unsupported; (5) sitting unsupported; (6) standing with eyes closed; (7) standing with feet together; (8) standing with one foot in front; (9) standing on one foot; (10) turning 360 degrees; (11) turning to look behind; (12) retrieving object from floor; (13) placing alternate foot on stool; (14) reaching forward with outstretched arm. All the children were evaluated following the sequence proposed by the scale. Evaluations were carried out in Rehabilitation Centers or child’s house. A trained examiner that previously achieved an intraobserver concordance of 85%, applied all the tests. 2.3. Data analysis Subjects’ PBS scores were analyzed through descriptive statistics to obtain mean values, standard deviance, and 95% confidence intervals for each GMFCS level. Subsequently, one-way analysis of variance (one-way ANOVA), followed by Tukey’s post hoc test, was used to determine PBS score divergence among GMFCS groups. The same sequence was reapplied to identify differences among GMFC groups for each of the 14 tasks evaluated by PBS. Finally, discriminant analysis was applied, using SPSS (version 17.0), to assess the capacity of PBS total scores to identify the GMFCS group to which subjects belonged. The significance level adopted for the statistical tests was 5%. 3. Results Participants’ characterization data in each of GMFCS groups and the confidence interval for the total scores are displayed in Table 1. The one-way ANOVA test indicated divergence in aggregate PBS total scores among GMFCS groups (F = 79.627; p < 0.01). The effect size found was high (0.92) and its power was 100%. Tukey’s post hoc test identified divergence in PBS total scores between GMFCS I and all other groups (p < 0.01) and GMFCS II and all others (p < 0.01). No difference, however, was found between groups III and IV (p = 0.291) or between groups IV and V (p = 0.591). Tukey’s post hoc test was applied to each of the 14 PBS tasks to identify differences among GMFCS groups. It was observed differences between levels I and II of GMFCS in the items 7, 8, 9, 10, 11 and 13 of the PBS. The differences between levels II and III were observed in items 1, 2, 4, 6, 7, 10 and 11. The difference observed between level III and IV were restricted to items 1, 2 and 3. We just observed differences in items 3 and 5 for the levels IV and V of GMFCS. These results can be observed in Table 2. Discriminant analysis was done to predict the GMFCS level of subjects from their PBS scores. Discriminant function identified that PBS scores account for 85.7% of the variation among GMFCS groups. In addition, cross-validated classification showed that 67% of the subjects could be classified appropriately in regard to GMFCS level from their PBS scores.
Table 1 Characteristics of the groups according to the Gross Motor Function Classification System (GMFCS), sample size, gender, age, motor impairment and confidence intervals (CI) of the Pediatric Balance Test (PBS) score. GMFCS group
Sample size
Gender
Age (years)
Motor impairment
PBS CI 95%
I
14
8 male 6 female
1021 (4.5)
13 Hemiplegia 1 Diplegia
38.3–51.4
II
11
8 male 3 female
9.54 (5.0)
4 Hemiplegia 6 Diplegia 1 Atetose
26.5–40.7
III
7
3 male 4 female
6.85 (1.9)
6 Diplegia 1 Tetraplegia
6.7–19.8
IV
9
3 male 6 female
8.11 (3.0)
1 Hemiplegia 2 Diplegia 6 Tetraplegia
3.4–7.6
17
14 male 3 female
8.70 (4.1)
1 Diplegia 16 Tetraplegia
0.01–1.7
V
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Table 2 Differences between Gross Motor Function Classification System (GMFCS) groups in each of the 14 activities of the Pediatric Balance Scale (PBS). The data are presented by means of the difference, confidence interval of the difference and p value. PBS activity
Differences between groups I and II
Differences between groups II and III
Differences between groups III and IV
Differences between groups IV and V
1 Sitting-to-standing
0.29 [ 0.51–1.10] p = 0.076
1.20 [0.23–2.18] p = 0.008*
1.76 [0.74–2.77] p = 0.000*
0.54 [ 0.28–1.37] p = 0.347
2 Standing-to sitting
0.10 [ 0.97–0.73] p = 0.997
1.67 [0.63–2.71] p = 0.000*
1.92 [ 3.00 to p = 0.000*
3 Transfers
0.27 [ 0.65–1.21] p = 0.914
0.74 [ 0.32–1.90] p = 0.279
1.57 [0.40–2.73] p = 0.003*
1.00 [0.04–1.95] p = 0.035*
4 Standing unsupported
0.42 [ 0.46–1.31] p = 0.667
2.64 [1.58–3.71] p = 0.000*
0.71 [ 0.39–1.82] p = 0.376
0.00 [ 0.90–0.90] p=1
5 Sitting unsupported
0.09 [ 0.88–1.06] p = 0.999
0.05 [1.11–1.22] p=1
0.19 [ 1.02–1.40] p = 0.992
2.9 [1.9–3.8] p = 0.00*
6 Standing with eyes closed
0.61 [ 0.58–1.80] p = 0.606
2.24 [0.80–3.68] p = 0.000*
0.57 [ 2.07–0.92] p = 0.818
0.00 [ 1.22–1.22] p=1
7 Standing with feet together
1.38 [0.24–2.53] p = 0.010*
2.03 [0.66–3.41] p = 0.001*
0.14 [ 1.29–1.57] p = 0.999
0.00 [ 1.17–1.17] p=1
8 Standing with one foot in front
1.34 [0.19–2.49] p = 0.014*
0.58 [ 0.79–1.96] p = 0.753
0.14 [ 1.29–1.57] p = 0.999
0.00 [ 1.17–1.17] p=1
9 Standing on one foot
1.74 [0.87–2.60] p = 0.000*
0.40 [ 0.63–1.43] p = 0.806
0.14 [ 0.93–1.22] p = 0.996
0.00 [ 0.88–0.88] p=1
10 Turning 360 degrees
1.45 [0.48–2.42] p = 0.001*
1.54 [0.37–2.71] p = 0.004*
0.00 [ 1.21–1.21] p=1
0.00 [ 0.99–0.99] p=1
11 Turning to look behind
1.05 [0.22–1.89] p = 0.006*
1.72 [0.72–2.72] p = 0.000*
0.00 [ 1.04–1.04] p=1
0.00 [ 0.85–0.85] p=1
12 Retrieving object from floor
0.29 [ 0.65–1.25] p = 0.902
2.70 [1.55–3.84] p = 0.000*
0.57 [ 0.62–1.76] p = 0.661
0.00 [ 0.97–0.97] p=1
13 Placing alternative foot on stool
1.27 [0.03–2.52] p = 0.042*
1.36 [ 0.13–2.86] p = 0.091
0.00 [ 1.56–1.56] p=1
0.00 [ 1.27–1.27] p=1
14 Reaching forward with outstreched arm
1.13 [ 0.05–2.32] p = 0.068
1.36 [ 0.06–2.79] p = 0.068
0.00 [ 1.48–1.48] p=1
0.00 [ 1.21–1.21] p=1
0.83]
0.22 [ 0.66–1.11] p = 0.954
4. Discussion The study sought to evaluate the functional balance of children with CP using PBS, to identify differences in PBS scores among these children at distinct GMFCS levels, to set confidence interval of PBS in each level of GMFC, and to assess whether PBS scores could be used to predict their GMFCS levels. The results indicate that GMFCS levels I, II, and III differ from each other in regard to functional balance scores, while groups III and IV and groups IV and V do not demonstrate significant divergence on PBS total scores. Results also indicated that PBS total scores are capable of discriminate GMFCS levels of children with CP. The GMFCS was developed to evaluate the degree of neuromotor impairment in children with CP by classifying their gross motor function with emphasis on sitting and walking movement without judging its quality (Palisano et al., 1997). Children classified at GMFCS levels I and II present mild motor impairment; level III, moderate impairment; and levels IV and V, severe impairment (Chagas et al., 2008; Palisano et al., 1997). Accordingly, the use of this classification system in conjunction with other evaluation tools facilitates the interpretation of children’s motor skills, providing a comprehensive view of functioning levels. As previously noted, the PBS total scores of the GMFCS level I and II groups differ. Among the major motor tasks that distinguish these levels are the capacities to balance and move intentionally and independently at level I but not at level II (Palisano, Cameron, Rosenbaum, Walter, & Russell, 2006). These are more complex motor tasks such as running and jumping, keeping balance when standing without support, and walking long distances. Children who demonstrate these abilities can more easily perform PBS tasks such as standing on one foot, standing without support in tandem prosecution, and rotating one’s body in place. Performance of PBS tasks involving standing with feet together (item 7), standing with one foot in front (item 8), standing on one foot (item 9), turning 360 degrees (item 10), turning to look behind (item 11), and placing alternative foot on stool (item13) revealed significant differences between GMFCS levels I and II. Therefore, the rehabilitations programs targeting to improve functional balance in children with CP GMFCS level II should emphasize the accomplishment of these tasks.
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Gan et al. did not find significant divergence in Berg Balance Scale scores for children with CP classified at GMFCS levels I and II (Gan, Tung, Tang, & Wang, 2008). The difference between the results of their study and the present one is related to the measurement tools used. Whereas Gan et al. (2008) used the Berg Balance Scale, which evaluates postural control in adults; the present study uses the PBS, which has been validated for use with children (Franjoine et al., 2003). The duration of postures required by the Berg Balance Scale appeared to be inadequate to detect differences in balance for children with CP classified at GMFCS levels I and II. With the validation of PBS for pediatric use, the evaluation of children’s balance has become more precise (Chen et al., 2013; Franjoine et al., 2003). In this study, the confidence interval was determined for PBS scores for each GMFCS level and differences between groups for each PBS task were assessed. Confidence intervals are a critical factor in evaluating functional balance in children with CP, since it sets acceptable variation values in the performance for each GMFCS level. The setting of confidence interval of PBS in each level of GMFC is an important measure to guide physical therapists in clinical practice. The establishment of intervals relating to PBS scores in which the levels of GMFCS are expected to punctuate allows the professionals to verify if the functional balance presented by the children is consistent with their GMFCS level. This evaluation ensures a better planning and performance of the proposed rehabilitation therapies. GMFCS levels II and III groups evidenced divergence in their PBS total scores. According to Palisano et al. (2006), these differences are related to independent indoor gait (Woollacott & Shumway-Cook, 2005). The present study found that the main differences between these groups involved the PBS tasks of sitting to standing (item 1) and standing to sitting (item 2), tasks that demand concentric-eccentric quadriceps muscle control, commonly compromised in children with neuromotor disorder (Nashner, Shumway-Cook, & Marin, 1983; Woollacott & Shumway-Cook, 2005). Other tasks exhibiting differences in scores between GMFCS groups II and III are standing unsupported (item 4), standing with eyes closed (item 6), standing with feet together (item 7), turning 360 degrees (item 10), turning to look behind (item 11), retrieving an object from the floor (item 12), and reaching forward with outstretched arm (item 14). These tasks require static and dynamic postural control, which are compromised in children with CP (Palisano et al., 2006; Pava˜o, Santos, Woollacott, & Rocha, 2013). Accordingly, children classified at GMFCS level III may encounter challenges in performing them, since they cannot walk without assistive mobility devices even indoors. Thus, children classified at GMFCS level II, who are able to walk indoors without support, are likely to attain higher scores on PBS tasks than those at level III, who cannot. As noted, the study found no significant PBS scores differences between groups classified at GMFCS levels III and IV or between levels IV and V. Primary functional differences related to groups III and IV regard independent mobility. Children classified at level III are able to sit with little or no support, and to walk with assistive mobile devices. They also exhibit greater independence in standing up than children at level IV, who usually require support to sit and have limited selfmobility. Study results indicate that subjects classified at GMFCS levels III and IV, while manifesting no significant divergence in PBS scores, demonstrated differences in the following PBS tasks: sitting to standing (item 1), standing to sitting (item 2), and transfers (item 3). In regard to the groups mentioned above, PBS does not evaluate a sufficiently broad range of tasks to distinguish them, as only one involves sitting unsupported (item 5). The study found that subjects in these groups differed only when standing to sitting was tested (item 2); this task may be executed by children at level IV with anterior support of the upper limbs, but is challenging for children at level V in the absence of head and trunk control. According to Palisano et al. (2006), the main functional differences at these levels involve head and trunk control while sitting, present at level IV and absent at level V. In the present study, it was observed that these groups are differentiated by their capacity to perform the following PBS tasks: transfers (3) and sitting unsupported (5), which children at level IV are capable of performing under supervision and with upper limb anterior support and those at level V are not. PBS, however, does not include tasks to evaluate trunk control while sitting other than transfers (item 3) and sitting unsupported (item 5). Study results corroborate Franjoine et al.’s validation of PBS as an instrument well suited to evaluating children with mild impairment (Franjoine et al., 2003). While PBS can distinguish the GMFCS levels of children with mild impairment from those with moderate, it is incapable of distinguishing children with moderate impairment from those with severe impairment. These results are likely related to the degree of motor impairment at each of the GMFCS levels, with levels III, IV, and V presenting significant levels of spasticity, muscle weakness, and poor postural control, impairing the performance of tasks requiring balance (Assumpc¸a˜o et al., 2011; Girolami et al., 2011; Nashner et al., 1983). For these highly impaired children, incapable of performing tasks that involve standing without support or require independent movement while standing, PBS tasks are insufficiently sensitive to detect differences between levels of GMFCS. These results figured out the importance of carefully choose appropriate instruments to evaluate balance in children with CP. It is important taking into account the motor impairments presented by the child to ensure reliability in balance tests. It is important to point that the tasks which revealed significant differences between the GMFCS groups should be reproduced in functional contexts during rehabilitation programs in order to improve functional balance of the children according to their GMFCS level. The further implementation of these tasks in functional activities performed in daily routine can improve balance and consequently social participation. Study results also affirm that PBS scores are capable of establishing GMFCS levels of children with CP. A total of 67% of the evaluated subjects could be appropriately rated by this means. In addition, the study found that PBS scores account for 85.7% of the variation among GMFCS groups. This indicates that the capacity to maintain balance in static postures and while
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executing dynamic activities is the primary factor in classifying gross motor function in children with CP, with other factors such as muscle force and muscle tone contributing to 33%. 5. Conclusion According to our findings PBS is a satisfactory instrument to assess balance in children with mild to moderate CP, able to detect differences between levels I, II and III of GMFCS. The instrument can also be used to establish GMFCS level of children with CP. The presented results allow us to better characterize functionality in children with CP according to GMFCS level by means of balance related parameters. They also enable to specify the expected tasks that are expected to be accomplished by the children in each level, contributing with therapeutic planning and monitoring. These results also support the importance of chooses appropriate instruments to evaluate balance in children with CP in order to get suitable results. Further studies using appropriate instruments to assess balance in moderate and severe impaired children with CP can be carried out with the purpose of verifying differences in total scores according to GMFCS levels. It is expected that this approach of connect balance assessment and motor function could better guide rehabilitation programs in children with CP. The chief limitation of the present study was the sample size. The sample size in each level of GMFCS could be more homogeneous. Funding The authors declare that the present article was not supported financially by a grant. References Assumpc¸a˜o, M. S., Piucco, E. C., Correˆa, E. C. R., & Ries, L. G. K. (2011). Coativac¸a˜o, espasticidade, desempenho motor e funcional na paralisia cerebral. Motriz, 17, 650–659. Barela, J. A., Focks, G. M. J., Hilgeholt, T., Barela, A. M. F., Carvalho, R. P., & Savelsbergh, G. J. P. (2011). Perception – action and adaptation in postural control of children and adolescents with cerebral palsy. 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Kembhavi, G., Darrah, J., Magill-Evans, J., & Loomis, J. (2002). Using the Berg Balance Scale to distinguish balance abilities in children with cerebral palsy. Pediatric Physical Therapy, 14, 92–99. Nashner, L. M., Shumway-Cook, A., & Marin, O. (1983). Stance posture control in select groups of children with cerebral palsy: Deficits in sensory organization and muscular coordination. Experimental Brain Research, 49, 393–409. Ostensjo, S., Carlberg, E. B., & Vollestad, N. K. (2004). Motor impairments in young children with cerebral palsy: Relationship to gross motor function and everyday activities. Developmental Medicine & Child Neurology, 46, 580–589. Palisano, R. J., Rosenbaum, P., Bartlett, D., & Livingston, M. H. (2008). Content validity of the expanded and revised gross motor function classification system. Developmental Medicine and Child Neurology, 50, 744–750. Palisano, R. J., Cameron, D., Rosenbaum, P. L., Walter, S. D., & Russell, D. (2006). 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Contents lists available at ScienceDirect
Research in Developmental Disabilities
Functional balance and gross motor function in children with cerebral palsy Silvia Leticia Pava˜o *, Kayo Andre F. Barbosa, Tatiana de Oliveira Sato, Nelci Adriana Cicuto Ferreira Rocha Department of Physiotherapy, Neuropediatrics Section, Federal University of Sa˜o Carlos, Rod. Washington Luis, km 235, 13565-905 Sa˜o Carlos-SP, Brazil
A R T I C L E I N F O
A B S T R A C T
Article history: Received 26 March 2014 Received in revised form 27 May 2014 Accepted 29 May 2014 Available online
Aims: To compare scores of children with cerebral palsy (CP) at different levels of Gross Motor Function Classification System (GMFCS), using the Pediatric Balance Scale (PBS) and to assess whether it can be used to predict GMFCS levels in children with CP. Methods: Fifty-eight children with CP levels I–V of GMFCS were assessed by PBS and grouped according to their GMFCS level. Results: It was observed differences in PBS scores between GMFCS I and II and between GMFCS II and III groups. Discriminant analysis indicated a 67% accuracy for the PBS instrument in assessing the GMFCS level of children with CP. Interpretation: PBS is able to detect differences among GMFCS levels I, II, and III of mild and moderate impairment. Accordingly, PBS can be used reliably in clinical practice to indicate the motor impairment level of such children. The results enable specify the expected tasks that are expected to be accomplished by the children in each GMFCS level, contributing with therapeutic planning and monitoring. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Cerebral palsy Pediatric Balance Scale GMFCS Postural control Scoring
1. Introduction Postural control demands the capacity to maintain center of mass within the limits of the support base and alignment of body segments (Castilho-Weinert & Forti-Bellani, 2011). Therefore, the performance of daily tasks such as self-care and mobility require postural control (Duarte & Freitas, 2010). Children with cerebral palsy (CP) besides presenting spasticity, muscular weakness, and adaptive modifications of muscle length (Assumpc¸a˜o, Piucco, Correˆa, & Ries, 2011), show a compromised capability to respond to loss of balance (Barela et al., 2011). Deficits in postural control in CP result from altered sensory processing and biomechanical alignment, which determine modified neuromuscular responses (Assumpc¸a˜o et al., 2011; Burtner, Qualls, & Woollacott, 1998; Woollacott et al., 1998). As these balance deficits impact the performance of daily activities (Ostensjo, Carlberg, & Vollestad, 2004), the assessment of postural control in children with CP is crucial to quantifying postural deficits, measuring rehabilitative progress, and also guide therapeutic interventions (Fig. 1). Several instruments have been validated for postural control evaluation including force plates (Ju, Hwang, & Cherng, 2012), electromyographic (Girolami, Shiratori, & Aruin, 2011) and joint angles analysis (Assumpc¸a˜o et al., 2011). The
* Corresponding author. Tel.: +55 16 3351 0467; fax: +55 16 3351 0467. E-mail address: [email protected] (S.L. Pava˜o). http://dx.doi.org/10.1016/j.ridd.2014.05.024 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
[(Fig._1)TD$IG]
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Fig. 1. Box plot of the total score of the Pediatric Balance Scale (PBS) among Gross Motor Function Classification System (GMFCS) groups.
complexity and cost of these instruments, however, significantly limit their use in clinical practice. Thus, the use of clinical scales such as the Pediatric Balance Scale (PBS) (Franjoine, Gunther, & Taylor, 2003; Reilly, Woollacott, van Donkelaar, & Saavedra, 2008) is simpler and may be a less expensive alternative to be used in clinical practice. PBS is a reliable instrument for assessment of functional balance in children with neuromotor impairments and assesses the elements of postural control that enable these children to perform daily activities effectively (Ries, Michaelsen, Soares, Monteiro, & Allegretti, 2012). Although PBS has been validated for use with such children (Franjoine et al., 2003; Ries et al., 2012) few studies have used it to evaluate balance in children with CP (Reilly et al., 2008) or have related PBS scores with GMFCS level in this population (Kembhavi, Darrah, Magill-Evans, & Loomis, 2002). Accordingly, the current study sought to evaluate the functional balance of children with CP using PBS, to identify differences in PBS total scores at distinct Gross Motor Function Classification System (GMFCS) levels, to set confidence intervals of PBS in each level of GMFCS and to assess whether PBS scores could be used as predictors of the GMFCS level in children with CP. Studying the differences in PBS total scores at distinct GMFCS levels, as well as assessing the PBS scores as predictors of the GMFCS level in children with CP will provide a broader understanding of balance abilities in each GMFCS level, specifying the expected tasks that are expected to be accomplished in each level. This approach will also facilitate the rehabilitation planning guiding some balance tasks to be accomplished by the children during physical therapy, as well as the measurement of clinical progress of the patients, since it can also predict the expected balance score the children must present according to their GMFCS level. 2. Methods 2.1. Participants The present study has a transversal design. Fifty-eight subjects (36 male, 22 female), with average age of 8.9 years (4.1), were selected at rehabilitation sites. All the included subjects were children with CP between 0 and 18 years old, and were involved in rehabilitation programs at least once a week. Written informed consent from the child’s legal guardian was also necessary. The study was authorized by the Ethics Committee for Research with Human Subjects of the Federal University of Sa˜o Carlos (protocol 363/2010). 2.2. Materials and procedure Children were classified according to GMFCS (Palisano et al., 1997) and divided into five groups according to their GMFCS level. GMFCS represents a functional classification of children with CP, which aims to determine the level of the child based
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on their abilities and limitations to perform gross motor function activities. Children can be classified according with five levels as follows: level I represents the ability to walk without limitations, level II indicates the ability to walk with limitations, level III is consisted of children that walk using a handheld mobility device; level IV includes children that present self-mobility with limitations, and level V is composed by children that are transported in a manual wheelchair (Palisano, Rosenbaum, Bartlett, & Livingston, 2008). Subjects’ functional balance was evaluated using the PBS (Franjoine et al., 2003). Derived from the Berg Balance Scale, which evaluates postural control in adults, PBS has been adapted and validated for the Brazilian population (Ries et al., 2012). PBS aggregate scores (hereafter PBS scores) for the 14 tasks evaluated can range from 0 to 56, with higher scores indicating better postural control. The evaluated tasks on PBS are the following: (1) sit to standing; (2) standing to sitting; (3) transfers; (4) standing unsupported; (5) sitting unsupported; (6) standing with eyes closed; (7) standing with feet together; (8) standing with one foot in front; (9) standing on one foot; (10) turning 360 degrees; (11) turning to look behind; (12) retrieving object from floor; (13) placing alternate foot on stool; (14) reaching forward with outstretched arm. All the children were evaluated following the sequence proposed by the scale. Evaluations were carried out in Rehabilitation Centers or child’s house. A trained examiner that previously achieved an intraobserver concordance of 85%, applied all the tests. 2.3. Data analysis Subjects’ PBS scores were analyzed through descriptive statistics to obtain mean values, standard deviance, and 95% confidence intervals for each GMFCS level. Subsequently, one-way analysis of variance (one-way ANOVA), followed by Tukey’s post hoc test, was used to determine PBS score divergence among GMFCS groups. The same sequence was reapplied to identify differences among GMFC groups for each of the 14 tasks evaluated by PBS. Finally, discriminant analysis was applied, using SPSS (version 17.0), to assess the capacity of PBS total scores to identify the GMFCS group to which subjects belonged. The significance level adopted for the statistical tests was 5%. 3. Results Participants’ characterization data in each of GMFCS groups and the confidence interval for the total scores are displayed in Table 1. The one-way ANOVA test indicated divergence in aggregate PBS total scores among GMFCS groups (F = 79.627; p < 0.01). The effect size found was high (0.92) and its power was 100%. Tukey’s post hoc test identified divergence in PBS total scores between GMFCS I and all other groups (p < 0.01) and GMFCS II and all others (p < 0.01). No difference, however, was found between groups III and IV (p = 0.291) or between groups IV and V (p = 0.591). Tukey’s post hoc test was applied to each of the 14 PBS tasks to identify differences among GMFCS groups. It was observed differences between levels I and II of GMFCS in the items 7, 8, 9, 10, 11 and 13 of the PBS. The differences between levels II and III were observed in items 1, 2, 4, 6, 7, 10 and 11. The difference observed between level III and IV were restricted to items 1, 2 and 3. We just observed differences in items 3 and 5 for the levels IV and V of GMFCS. These results can be observed in Table 2. Discriminant analysis was done to predict the GMFCS level of subjects from their PBS scores. Discriminant function identified that PBS scores account for 85.7% of the variation among GMFCS groups. In addition, cross-validated classification showed that 67% of the subjects could be classified appropriately in regard to GMFCS level from their PBS scores.
Table 1 Characteristics of the groups according to the Gross Motor Function Classification System (GMFCS), sample size, gender, age, motor impairment and confidence intervals (CI) of the Pediatric Balance Test (PBS) score. GMFCS group
Sample size
Gender
Age (years)
Motor impairment
PBS CI 95%
I
14
8 male 6 female
1021 (4.5)
13 Hemiplegia 1 Diplegia
38.3–51.4
II
11
8 male 3 female
9.54 (5.0)
4 Hemiplegia 6 Diplegia 1 Atetose
26.5–40.7
III
7
3 male 4 female
6.85 (1.9)
6 Diplegia 1 Tetraplegia
6.7–19.8
IV
9
3 male 6 female
8.11 (3.0)
1 Hemiplegia 2 Diplegia 6 Tetraplegia
3.4–7.6
17
14 male 3 female
8.70 (4.1)
1 Diplegia 16 Tetraplegia
0.01–1.7
V
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Table 2 Differences between Gross Motor Function Classification System (GMFCS) groups in each of the 14 activities of the Pediatric Balance Scale (PBS). The data are presented by means of the difference, confidence interval of the difference and p value. PBS activity
Differences between groups I and II
Differences between groups II and III
Differences between groups III and IV
Differences between groups IV and V
1 Sitting-to-standing
0.29 [ 0.51–1.10] p = 0.076
1.20 [0.23–2.18] p = 0.008*
1.76 [0.74–2.77] p = 0.000*
0.54 [ 0.28–1.37] p = 0.347
2 Standing-to sitting
0.10 [ 0.97–0.73] p = 0.997
1.67 [0.63–2.71] p = 0.000*
1.92 [ 3.00 to p = 0.000*
3 Transfers
0.27 [ 0.65–1.21] p = 0.914
0.74 [ 0.32–1.90] p = 0.279
1.57 [0.40–2.73] p = 0.003*
1.00 [0.04–1.95] p = 0.035*
4 Standing unsupported
0.42 [ 0.46–1.31] p = 0.667
2.64 [1.58–3.71] p = 0.000*
0.71 [ 0.39–1.82] p = 0.376
0.00 [ 0.90–0.90] p=1
5 Sitting unsupported
0.09 [ 0.88–1.06] p = 0.999
0.05 [1.11–1.22] p=1
0.19 [ 1.02–1.40] p = 0.992
2.9 [1.9–3.8] p = 0.00*
6 Standing with eyes closed
0.61 [ 0.58–1.80] p = 0.606
2.24 [0.80–3.68] p = 0.000*
0.57 [ 2.07–0.92] p = 0.818
0.00 [ 1.22–1.22] p=1
7 Standing with feet together
1.38 [0.24–2.53] p = 0.010*
2.03 [0.66–3.41] p = 0.001*
0.14 [ 1.29–1.57] p = 0.999
0.00 [ 1.17–1.17] p=1
8 Standing with one foot in front
1.34 [0.19–2.49] p = 0.014*
0.58 [ 0.79–1.96] p = 0.753
0.14 [ 1.29–1.57] p = 0.999
0.00 [ 1.17–1.17] p=1
9 Standing on one foot
1.74 [0.87–2.60] p = 0.000*
0.40 [ 0.63–1.43] p = 0.806
0.14 [ 0.93–1.22] p = 0.996
0.00 [ 0.88–0.88] p=1
10 Turning 360 degrees
1.45 [0.48–2.42] p = 0.001*
1.54 [0.37–2.71] p = 0.004*
0.00 [ 1.21–1.21] p=1
0.00 [ 0.99–0.99] p=1
11 Turning to look behind
1.05 [0.22–1.89] p = 0.006*
1.72 [0.72–2.72] p = 0.000*
0.00 [ 1.04–1.04] p=1
0.00 [ 0.85–0.85] p=1
12 Retrieving object from floor
0.29 [ 0.65–1.25] p = 0.902
2.70 [1.55–3.84] p = 0.000*
0.57 [ 0.62–1.76] p = 0.661
0.00 [ 0.97–0.97] p=1
13 Placing alternative foot on stool
1.27 [0.03–2.52] p = 0.042*
1.36 [ 0.13–2.86] p = 0.091
0.00 [ 1.56–1.56] p=1
0.00 [ 1.27–1.27] p=1
14 Reaching forward with outstreched arm
1.13 [ 0.05–2.32] p = 0.068
1.36 [ 0.06–2.79] p = 0.068
0.00 [ 1.48–1.48] p=1
0.00 [ 1.21–1.21] p=1
0.83]
0.22 [ 0.66–1.11] p = 0.954
4. Discussion The study sought to evaluate the functional balance of children with CP using PBS, to identify differences in PBS scores among these children at distinct GMFCS levels, to set confidence interval of PBS in each level of GMFC, and to assess whether PBS scores could be used to predict their GMFCS levels. The results indicate that GMFCS levels I, II, and III differ from each other in regard to functional balance scores, while groups III and IV and groups IV and V do not demonstrate significant divergence on PBS total scores. Results also indicated that PBS total scores are capable of discriminate GMFCS levels of children with CP. The GMFCS was developed to evaluate the degree of neuromotor impairment in children with CP by classifying their gross motor function with emphasis on sitting and walking movement without judging its quality (Palisano et al., 1997). Children classified at GMFCS levels I and II present mild motor impairment; level III, moderate impairment; and levels IV and V, severe impairment (Chagas et al., 2008; Palisano et al., 1997). Accordingly, the use of this classification system in conjunction with other evaluation tools facilitates the interpretation of children’s motor skills, providing a comprehensive view of functioning levels. As previously noted, the PBS total scores of the GMFCS level I and II groups differ. Among the major motor tasks that distinguish these levels are the capacities to balance and move intentionally and independently at level I but not at level II (Palisano, Cameron, Rosenbaum, Walter, & Russell, 2006). These are more complex motor tasks such as running and jumping, keeping balance when standing without support, and walking long distances. Children who demonstrate these abilities can more easily perform PBS tasks such as standing on one foot, standing without support in tandem prosecution, and rotating one’s body in place. Performance of PBS tasks involving standing with feet together (item 7), standing with one foot in front (item 8), standing on one foot (item 9), turning 360 degrees (item 10), turning to look behind (item 11), and placing alternative foot on stool (item13) revealed significant differences between GMFCS levels I and II. Therefore, the rehabilitations programs targeting to improve functional balance in children with CP GMFCS level II should emphasize the accomplishment of these tasks.
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Gan et al. did not find significant divergence in Berg Balance Scale scores for children with CP classified at GMFCS levels I and II (Gan, Tung, Tang, & Wang, 2008). The difference between the results of their study and the present one is related to the measurement tools used. Whereas Gan et al. (2008) used the Berg Balance Scale, which evaluates postural control in adults; the present study uses the PBS, which has been validated for use with children (Franjoine et al., 2003). The duration of postures required by the Berg Balance Scale appeared to be inadequate to detect differences in balance for children with CP classified at GMFCS levels I and II. With the validation of PBS for pediatric use, the evaluation of children’s balance has become more precise (Chen et al., 2013; Franjoine et al., 2003). In this study, the confidence interval was determined for PBS scores for each GMFCS level and differences between groups for each PBS task were assessed. Confidence intervals are a critical factor in evaluating functional balance in children with CP, since it sets acceptable variation values in the performance for each GMFCS level. The setting of confidence interval of PBS in each level of GMFC is an important measure to guide physical therapists in clinical practice. The establishment of intervals relating to PBS scores in which the levels of GMFCS are expected to punctuate allows the professionals to verify if the functional balance presented by the children is consistent with their GMFCS level. This evaluation ensures a better planning and performance of the proposed rehabilitation therapies. GMFCS levels II and III groups evidenced divergence in their PBS total scores. According to Palisano et al. (2006), these differences are related to independent indoor gait (Woollacott & Shumway-Cook, 2005). The present study found that the main differences between these groups involved the PBS tasks of sitting to standing (item 1) and standing to sitting (item 2), tasks that demand concentric-eccentric quadriceps muscle control, commonly compromised in children with neuromotor disorder (Nashner, Shumway-Cook, & Marin, 1983; Woollacott & Shumway-Cook, 2005). Other tasks exhibiting differences in scores between GMFCS groups II and III are standing unsupported (item 4), standing with eyes closed (item 6), standing with feet together (item 7), turning 360 degrees (item 10), turning to look behind (item 11), retrieving an object from the floor (item 12), and reaching forward with outstretched arm (item 14). These tasks require static and dynamic postural control, which are compromised in children with CP (Palisano et al., 2006; Pava˜o, Santos, Woollacott, & Rocha, 2013). Accordingly, children classified at GMFCS level III may encounter challenges in performing them, since they cannot walk without assistive mobility devices even indoors. Thus, children classified at GMFCS level II, who are able to walk indoors without support, are likely to attain higher scores on PBS tasks than those at level III, who cannot. As noted, the study found no significant PBS scores differences between groups classified at GMFCS levels III and IV or between levels IV and V. Primary functional differences related to groups III and IV regard independent mobility. Children classified at level III are able to sit with little or no support, and to walk with assistive mobile devices. They also exhibit greater independence in standing up than children at level IV, who usually require support to sit and have limited selfmobility. Study results indicate that subjects classified at GMFCS levels III and IV, while manifesting no significant divergence in PBS scores, demonstrated differences in the following PBS tasks: sitting to standing (item 1), standing to sitting (item 2), and transfers (item 3). In regard to the groups mentioned above, PBS does not evaluate a sufficiently broad range of tasks to distinguish them, as only one involves sitting unsupported (item 5). The study found that subjects in these groups differed only when standing to sitting was tested (item 2); this task may be executed by children at level IV with anterior support of the upper limbs, but is challenging for children at level V in the absence of head and trunk control. According to Palisano et al. (2006), the main functional differences at these levels involve head and trunk control while sitting, present at level IV and absent at level V. In the present study, it was observed that these groups are differentiated by their capacity to perform the following PBS tasks: transfers (3) and sitting unsupported (5), which children at level IV are capable of performing under supervision and with upper limb anterior support and those at level V are not. PBS, however, does not include tasks to evaluate trunk control while sitting other than transfers (item 3) and sitting unsupported (item 5). Study results corroborate Franjoine et al.’s validation of PBS as an instrument well suited to evaluating children with mild impairment (Franjoine et al., 2003). While PBS can distinguish the GMFCS levels of children with mild impairment from those with moderate, it is incapable of distinguishing children with moderate impairment from those with severe impairment. These results are likely related to the degree of motor impairment at each of the GMFCS levels, with levels III, IV, and V presenting significant levels of spasticity, muscle weakness, and poor postural control, impairing the performance of tasks requiring balance (Assumpc¸a˜o et al., 2011; Girolami et al., 2011; Nashner et al., 1983). For these highly impaired children, incapable of performing tasks that involve standing without support or require independent movement while standing, PBS tasks are insufficiently sensitive to detect differences between levels of GMFCS. These results figured out the importance of carefully choose appropriate instruments to evaluate balance in children with CP. It is important taking into account the motor impairments presented by the child to ensure reliability in balance tests. It is important to point that the tasks which revealed significant differences between the GMFCS groups should be reproduced in functional contexts during rehabilitation programs in order to improve functional balance of the children according to their GMFCS level. The further implementation of these tasks in functional activities performed in daily routine can improve balance and consequently social participation. Study results also affirm that PBS scores are capable of establishing GMFCS levels of children with CP. A total of 67% of the evaluated subjects could be appropriately rated by this means. In addition, the study found that PBS scores account for 85.7% of the variation among GMFCS groups. This indicates that the capacity to maintain balance in static postures and while
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executing dynamic activities is the primary factor in classifying gross motor function in children with CP, with other factors such as muscle force and muscle tone contributing to 33%. 5. Conclusion According to our findings PBS is a satisfactory instrument to assess balance in children with mild to moderate CP, able to detect differences between levels I, II and III of GMFCS. The instrument can also be used to establish GMFCS level of children with CP. The presented results allow us to better characterize functionality in children with CP according to GMFCS level by means of balance related parameters. They also enable to specify the expected tasks that are expected to be accomplished by the children in each level, contributing with therapeutic planning and monitoring. These results also support the importance of chooses appropriate instruments to evaluate balance in children with CP in order to get suitable results. Further studies using appropriate instruments to assess balance in moderate and severe impaired children with CP can be carried out with the purpose of verifying differences in total scores according to GMFCS levels. It is expected that this approach of connect balance assessment and motor function could better guide rehabilitation programs in children with CP. The chief limitation of the present study was the sample size. The sample size in each level of GMFCS could be more homogeneous. Funding The authors declare that the present article was not supported financially by a grant. References Assumpc¸a˜o, M. S., Piucco, E. C., Correˆa, E. C. R., & Ries, L. G. K. (2011). Coativac¸a˜o, espasticidade, desempenho motor e funcional na paralisia cerebral. Motriz, 17, 650–659. Barela, J. A., Focks, G. M. J., Hilgeholt, T., Barela, A. M. F., Carvalho, R. P., & Savelsbergh, G. J. P. (2011). Perception – action and adaptation in postural control of children and adolescents with cerebral palsy. 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