Reliability of the Gross Motor Function Classification System Expanded and Revised ( GMFCS E & R ) among students and health professionals in Brazil

142 Mailing address: Luzia Iara Pfeifer – Departamento de Neurociências e Ciências do Comportamento – Av. Bandeirantes, 3900 – Ribeirão Preto (SP), Brazil – CEP: 14049-900 Phone: +55 (16) 3315-4694 – E-mail: luziara@fmrp.usp.br – Financing source: Conselho Nacional de Desenvolvimento Científico e Tecnológico (scholar Larissa Bombarda Dias) Conflict of interest: Nothing to declare – Presentation: Dec. 2014 – Accepted for publication: May 2016 – Approved by the Research Ethics Committee of the hospital (HCRP no. 12469/2008). DOI: 10.1590/1809-2950/14396823022016


INTRODUCTION
Cerebral palsy comprises a group of permanent disorders of the development of movement and posture, causing activity limitation attributed to non-progressive disturbances that occurred in the developing fetal or infant brain.The motor disorders of cerebral palsy are often accompanied by disturbances of sensation, perception, cognition, communication, and behavior, by epilepsy, and by secondary musculoskeletal problems 1 .The severity of neuromuscular and musculoskeletal impairments associated with cerebral palsy is extremely variable and, consequently, motor function ranges from the ability to walk in the community and perform skills associated with play and recreation (e.g.run, jump) to complete dependence on caregiver assistance for selfcare and mobility 2 .The classifications of cerebral palsy are based on different approaches, such as the predominant motor abnormality (spastic, dyskinetic, ataxic), topographical distribution (unilateral and bilateral for spasticity), and functionality 1 .Due to the heterogeneity of cerebral palsy, it is common to find children with spastic CP that exhibit dystonia characteristics, as well as those with unilateral involvement with some degree of motor involvement on the opposite side, and others with bilateral involvement and asymmetry in both sides 1 .In addition, such traditional classification systems related to topography and motor abnormalities, although useful for clinical and epidemiological proposals, provide limited information about mobility, not indicating the severity level and, therefore, are not very helpful to the prognosis 3 .Thus, the classification of cerebral palsy should be accompanied by functional classifications 1 such as the Gross Motor Function Classification System (GMFCS) 4 .
The GMFCS is a five-level classification system based on voluntary movements, with emphasis on sitting, transportation, and mobility.Level I includes children and young people who walk without limitations; in level II the child has limitations to walk long distances and at equilibrium; in level III, the child walks using a handheld mobility device (walker, crutches, canes).Children and young people in level IV are usually transported in a manual or motorized wheelchair.In level V, there are severe head and trunk control limitations, requiring extensive use of assisted technology and physical assistance 4 .The GMFCS includes 4 age groups: 0 to 2 years, 2 to 4 years, 4 to 6 years, and 6 to 12 years 4 , and it was adapted transculturally to Brazilian Portuguese 5 .
The expanded and revised version of the GMFCS (GMFCS E&R) includes the age group from 12 to 18 years, which emphasizes that the performance of the gross motor function is influenced by physical, social, and attitudinal environment, and by personal factors such as preferences, interests, and motivation 6 .The GMFCS E&R translation into Brazilian Portuguese made in accordance with the ones suggested by Center For Childhood Disability Research (CanChild) and made available on their website * was conducted in 2010 by a group of occupational therapists and one neurologist 7 .
The validity and reliability of the original version of the GMFCS have been extensively studied and well established among health professionals in different countries (physical therapists, pediatricians, orthopedists, physiatrists, and occupational therapists) 6,8,9,10 , and parents 8,[11][12][13][14][15] , which is also beginning to occur with the extended and revised version (GMFCS E&R) 16 .The GMFCS can easily be incorporated into clinical practice, allowing comparisons of children accompanied by different clinicians with similar functional levels, and also can predict the gross motor function of children with cerebral palsy 17 .Moreover, it can be used by students, helping them to understand the heterogeneity of cerebral palsy, as it is a simple classification that does not require specific training 18 .Morris and Bartlett 18 mention that the use of videos of GMFCS allows students to understand that cerebral palsy comprises more than one motor type or topographical distribution, and show that a child with quadriplegia (bilateral spastic CP) can be classified into different levels of GMFCS (II, III, IV or V) 18 .
Although the GMFCS and the GMFCS E&R consist in classifications of easy application, studies that assess their reliability in Brazil are scarce 5,19 and did not verify their validity with other health professionals with different levels of experience in the area (strata) 20 , including undergraduate students, who are involved in the treatment of children with cerebral palsy.The aim of this study was to evaluate the reliability of the Portuguese version (Brazil) of the GMFCS E&R for students and health professionals (physical and occupational therapists), with different levels of experience.

METHODOLOGY
This is a cross-sectional and quantitative study that aimed to compare the classification of the gross motor function of children with cerebral palsy by students and health professionals (physical and occupational therapists with different levels of experience).This study was approved by the Research Ethics Committee * Avaiable from: www.canchild.ca.
of the Hospital das Clínicas of the Medical School of Ribeirão Preto.The parents signed an informed consent form (HCRP no.12469/2008).

PARTICIPANTS
Thirty children with cerebral palsy who frequented the neurology or rehabilitation service of a university hospital in São Paulo's countryside participated in the research from February to October 2011, aged between 4 and 18 years.Inclusion criteria were: to have the diagnosis of cerebral palsy, regardless of type and motor impairment, to be between 4 and 18 years, and to understand simple commands.Exclusion criteria were low vision or blindness and epilepsy.
Students and both physical and occupational therapists also participated in the study and composed three groups: Group 1) one occupational and one physical therapist graduated for more than 5 years with experience in neurology and in using the GMFCS; Group 2) one occupational and one physical therapist graduated for less than 2 years, who worked with neurology and had brief experience in using the GMFCS; Group 3) one senior student of occupational therapy and one senior student of physiotherapy from a public university of São Paulo's countryside, given that only the occupational therapy student had contact with the GMFCS to classify a child's motor level, as part of an academic activity.

DATA COLLECTION PROCEDURE
The children were assessed regarding the control of head, trunk, postural changes (scrolling, dragging, crawling, lying to sitting, sitting to standing), gait, and the parents were asked about the methods of mobility often used in internal and external environments (school, community).These assessments were conducted by an undergraduate student of occupational therapy of Group 3 and filmed by a research assistant.
The videos of the 30 children were sent to the participants of the three groups for classification of the motor level using the GMFCS E & R, and the children were identified by code and age.Students and professionals also received the GMFCS E & R translated into Brazilian Portuguese, having 15 days to complete the classification.The classifications of the groups' members were compared with that of an occupational therapist with 9 years of experience in neurology, who had previous contact with the GMFCS.

STATISTICAL ANALYSIS
The GMFCS E & R is a five-level ordinal scale, whose data were analyzed using the statistical test of not-weighted kappa with 95% confidence interval to examine the agreement among the groups, with different levels of experience (students and health professionals).

RESULTS
The average age of the children was 7.58 years (7 years and 7 months), ranging from 4 to 17.91 years.Most children had bilateral spastic CP (n=23), five had unilateral spastic CP, and two had dyskinetic CP.Regarding sex, 43.3% of the sample was composed of girls and 56.7% of boys.Table 1 shows the distribution of the types of cerebral palsy, age, and sex as a function of the levels of the GMFCS E & R. Children with unilateral spastic cerebral palsy were classified by the occupational therapist with greater experience in the level I of the GMFCS E & R, while children with bilateral spastic CP were distributed in all motor levels.
Table 2 shows the disagreements among the groups of professionals and students about the levels of the GMFCS E&R and the index of agreement among them (K).We found a total of 28 disagreements among the 3 assessed groups, which predominated between levels I and II (n=10) and III and IV (n=9).The agreement was almost perfect in Group 1 which involved professionals with the highest level of experience in the field of neurology, and substantial in other groups with less experience.

DISCUSSION
The Gross Motor Function Classification System (GMFCS) has been widely used in research and clinical practice, being a valid and reliable instrument to assess the gross motor function of children with cerebral palsy 4,22 .The results of this study indicated almost perfect agreement between physical and occupational therapists with more than 5 years of experience in neurology (Group 1), in which they classified the motor level of children using the Brazilian version of the GMFCS E & R. Results similar to this were obtained only in the Brazilian study developed by Silva et al. 19 (K=0.90), in which direct observation was held and the parents were questioned about methods of mobility for the motor level classification, involving one undergraduate student of OT and one occupational therapist with nine years of experience.
In this study, we found substantial agreement among students (Group 3) or professionals of the same area, with up to two years of experience (Group 2), when they classified the motor level of children using the Brazilian version of the GMFCS E&R.In most studies, the agreement in the classification of the GMFCS has also been substantial, with kappa coefficient raging between 0.64 and 0.80 4,9,12 , involving different health professionals (physical therapists 4,10,12,14,17 , doctors 8,9,10,17 , occupational therapists 4,5 , speech therapists 10 , and nurses 10 ) and different methods of collecting information to classify the gross motor function using the GMFCS or GMFCS E & R (direct observation 4,8,9,12,16 , questioning of parents 12,16 , review of medical records 7,8,23 ).
Indexes of agreement quite similar to the students' group of this research (Group 3) were obtained in other studies, but with more experienced professionals 8,10,12,23 .The study of Kondo et al. 10 involved professionals from different areas (physical therapists, occupational therapists, speech therapists, doctors, and nurses) who made direct observation of the child, with kappa of 0.66.The study of McDowell et al. 12 involved two physical therapists and direct observation of the child was also held associated with the questioning of the parents, with kappa of 0.64.
Although in our research the professional experience is related to a higher rate of reliability, in the aforementioned studies 10,12 , which involved health professionals, the agreement was similar to the students' group from our research, suggesting that professional experience is not the only determining factor for greater reliability in GMFCS classification.Besides the experience of the examiner, it is important to consider the method of gathering information, since research has shown that the index of agreement of GMFCS classification, using only the review of medical records, is lower, even when it involved health professionals from different areas 8,23 , in contrast to the studies that have done direct observation of the child and gathered information from the parents.In the study of Morris et al. 8 , the children were classified with the GMFCS by orthopedic surgeons through the review of medical records, obtaining fair agreement rates (k=0.38),while physical therapists and pediatricians classified the same children through direct observation associated with the review of medical records, obtaining a substantial agreement (k=0.65).We can verify that GMFCS and GMFCS E&R have shown to be reliable when used by health professionals of different areas and levels of professional experience, being the method of collecting information mostly accomplished through direct observation 4,8,9,12,16 and questioning of the parents 12,16 .
In this research, most disagreements in the classification of GMFCS E&R occurred between the levels I and II, and levels III and IV.The studies of McDowell et al. 12 , and Benedict et al. 23 also obtained disagreements, for the most part, between the levels with lower motor severity for children aged 4 years or older.Other studies already indicate a predominance of disagreements between levels that indicate higher motor severity (IV and V) for children in this age group or older 9,10 .
This research contributes to enlarge reliability studies of the GMFCS E&R in Brazil by professionals with different strata/levels of experience, reinforcing the idea that it can be used even by undergraduate students.Thus, the inclusion of this subject in undergraduate disciplines related to pediatric neurology can also assist students in understanding the heterogeneity of clinical types, levels of involvement and, mainly, the motor prognosis of children with cerebral palsy.This could be verified, for example, by looking at the description of the GMFCS E&R about the children in level V, who have severe limitations in maintaining antigravity head and trunk postures 6 , being necessary, therefore, the indication and use of assistive technology resources, such as wheelchairs and orthosis.
In addition, because the GMFCS is stable over time 24 it is possible to increase the communication between professionals and family members -helping them to understand the child's current skills -, discussing prognosis and planning future interventions, as well as improving public policies regarding this population 23 .

CONCLUSION
The Brazilian version of the GMFCS E&R (Brazil) proved reliable for use by health professionals (physical and occupational therapists), with different levels of experience, including undergraduate students.
Gross Motor Function, traduzido para o português como Sistema de Classificação da Função

Table 1 .
Distribution of the types of CP, age, and sex as a function of motor levels

Table 2 .
Disagreement among the groups as a function of GMFCS' levels, kappa coefficient, and confidence intervals (CI).