Grecco, Luanda André Collange MS; de Freitas, Tatiana Beline PT; Satie, Julia PT; Bagne, Eduardo PT; Oliveira, Claudia Santos PhD; de Souza, Daniel Rubio MD
Cerebral palsy (CP) is a blanket term for a group of permanent but mutable motor development disorders stemming from a primary brain lesion, causing secondary musculoskeletal alterations and limitations to activities of daily living.1 Motor impairments are the main manifestations of CP and affect the biomechanics of the body.2,3
Orthopedic surgeons play an important role in the management of secondary conditions resulting from CP.4 Surgical intervention for the lower limbs, especially during the years of development, is performed to improve gait patterns and functional capacity as well as to alleviate pain and improve positioning, thereby facilitating care given to the child.4–7 Among children with a capacity for gait (levels I to IV of the Gross Motor Function Classification System [GMFCS]),8,9 excessive flexion of the hip and knee, adduction and internal rotation of the hip, and an equinus foot may be indications for surgery when such conditions compromise performance of functional activities and gait or cause pain.4–8 Depending on the type and severity of the deformity and considering the age of the child, surgery may involve the soft tissues, such as a muscle-lengthening procedure, or bone, such as derotational osteotomies. Such surgery often results in prolonged immobilization during the period of tissue healing.4,7 The immobilization method and duration are decided by the orthopedist. Immobilization may be accomplished with braces or casts. The duration primarily depends on the type of surgery and the severity of each case.9 Children who undergo soft tissue surgery tend to remain immobilized for a shorter length of time (3–6 weeks) than those who have undergone bone procedures (4–12 weeks).
Children with CP do not participate in physical activities with sufficient intensity to develop cardiopulmonary fitness, endurance, and muscle strength, which leads to a continuous cycle of deconditioning and diminished functional abilities.10,11 Moreover, the systemic problems of deconditioning are aggravated by the aforementioned surgical procedures and consequent period of prolonged immobilization. Assisting the patient in establishing motor control in the new biomechanical alignment provided by the surgical procedure and promoting better physical fitness are major goals of postoperative physical therapy.
A number of strategies have been used to improve selective motor control and muscle coordination during gait to allow a greater degree of physical activity among individuals with CP.12–14 In recent years, gait training on a treadmill has been used in the physical therapeutic treatment of children with CP. A treadmill can be used with or without body-weight support and is designed for the training of a specific task with multiple repetitions of the different phases of gait.15–22 A recent systematic review of the literature demonstrated that treadmill training improves both the function of the lower limbs and spatiotemporal gait variables in children with CP.23 However, a number of limitations are pointed out in the current evidence on this subject, such as the small number of studies and the clinical diversity of the samples. Moreover, no studies have analyzed the effects of treadmill training on children with CP following orthopedic surgery in the lower limbs.
The aim of this study was to determine the effect of treadmill training on gross motor function and functional mobility in children and adolescents with CP in a physical therapy program following orthopedic surgery in the lower limbs. A further aim was to compare the results obtained with children having undergone soft tissue surgery alone with those who have undergone both soft tissue and bone surgery, with a consequently longer immobilization time.
This study received approval from the Human Research Ethics Committee of the Nove de Julho University (Brazil) and the Associação de Assistência à Criança Deficiente (Brazil) under process number 201862/2008 in compliance with the guidelines of Resolution 196/96 of the Brazilian Health Board. All parents/guardians signed a statement of informed consent agreeing to their children's participation.
A prospective, analytical study was carried out in 2010 involving children with CP participating in a physical therapy program following orthopedic surgery in the lower limbs. The following were the inclusion criteria: age between 8 and 15 years; levels II or III of the GMFCS8; and having undergone orthopedic surgery to improve the child's gait pattern. The following were the exclusion criteria: visual or cognitive impairment that would limit the execution of the study tasks; associated cardiopulmonary disease; postoperative complications (bone consolidation difficulties, infection, or pressure ulcers) and locomotion mainly using a wheelchair (without functional gait) in the preoperative period.
The sample was subdivided into 2 groups to determine whether the effects of treadmill training are influenced by the type of surgical procedure. The initial evaluation revealed that the children who underwent both soft tissue and bone surgery remained immobilized, on average, for twice the time as those who underwent soft tissue surgery alone. Group 1 comprised those having undergone surgical procedures involving only the soft tissues (muscle lengthening) and remaining immobilized for a maximum of 45 days. Group 2 included children having undergone surgical procedures involving both soft tissue and bone (derotational osteotomy of the femur and/or tibia; femur extending osteotomy and bone procedures on the feet) and immobilized for more than 45 days. Immobilization was considered the time elapsed between surgery and the removal of the cast, with consequent approval to undergo physical therapy. Figure 1 displays a flowchart of the study.
The participants were tested twice—once before and once after gait training. The tests were performed by a single examiner who was blinded to the aims and methods of the study. Each testing session consisted of measurement of anthropometric characteristics (body mass, height) and calculation of body mass index; the determination of gross motor function using the Gross Motor Function Measure–88 (GMFM-88),24,25 the 6-Minute Walk Test (6MWT),26,27 and a treadmill test of exercise effort.
Gross Motor Function Measure–88
The GMFM-88 is used to perform quantitative assessment of gross motor function in individuals with CP and has demonstrated validity and reliability. The measure is comprised of 88 items distributed among 5 subscales: (1) lying down and rolling; (2) sitting; (3) crawling and kneeling; (4) standing; and (5) walking, running, and jumping. The items on each subscale receive a score of 0 to 3 points, with higher scores denoting better performance.24,25
6-Minute Walk Test
The 6MWT is a reliable measure for the assessment of physical fitness and functional mobility in children with CP.26,27 This test quantifies functional mobility based on the distance (in meters) traveled in 6 minutes. In the present study, the 6MWT was carried out in compliance with the guidelines established by Maher et al26 and Thompson et al.27
There is no standardized treadmill test for the pediatric population with neurological disorders. The most often employed test in pediatrics is the modified Bruce protocol. However, this includes inclination of the treadmill, which makes it extremely difficult for children with moderate to severe motor impairment. This study used the symptom-limited cardiopulmonary effort test on a treadmill (Imbramed Mileniun ATL), using the ramp protocol with increasing speed (initially 0.5 km/h and increased 0.5 km/h each minute). The following were the criteria for interrupting the test: subjective sensation of fatigue, lower limb pain reported by the child, complex heart arrhythmia, a sudden increase or drop in blood pressure, an increase above maximal heart rate (HR) predicted for age of the individual, intense shortness of breath, and a drop in oxygenation accompanied by electrocardiographic alterations or signs and symptoms. At each stage of the test, the children were asked about shortness of breath and lower limb pain and the subjective responses were classified using the Borg Rating of Perceived Exertion Scale. During the test, blood pressure was measured using the left arm with a portable sphygmomanometer and stethoscope for indirect auscultation. The monitoring of electrocardiographic activity was performed with an Ecafix monitor, and HR was monitored with a Polar Electro Oy HR meter. Oxygen saturation (SpO2) was monitored continuously during the treadmill test using a portable oximeter (Nonin 8500A).
During the 6MWT (immediately before [after 20 minutes of rest] and immediately after the 6MWT) and treadmill test, the following measurements were obtained: HR, respiratory rate (RR), SpO2, systolic blood pressure (SBP), diastolic blood pressure (DBP), maximal velocity on the treadmill test, and distance traveled on the 6MWT.
The tests were distributed among 3 nonconsecutive days and performed in random order. Test sessions were carried out 1 week prior to and 1 week following gait training.
All participants began treadmill training after 8 weeks of postoperative physical therapy, following medical permission to stand and walk. Eight weeks of physical therapy were provided to allow the child to adapt to therapy without pain. During this period, the children performed 2 weekly 60-minute sessions of physical therapy. Each session consisted of passive movement of the lower limbs (5 minutes), muscle stretching exercises (especially the muscles affected by the surgery) (10 minutes), muscle strengthening exercises (active resistance exercises) (10 minutes), posture change training (movement from sitting to standing) (10 minutes), and standing and gait training on a fixed, flat surface (floor) (20 minutes).
Training was carried out on a treadmill (Imbramed Mileniun ATL) without partial weight support. The first 2 sessions were considered adaptation to the treadmill and involved 10 minutes of walking. The protocol consisted of 12 weeks of gait training (1 session per week), with a maximal duration of 30 minutes at 80% of the maximal velocity achieved on the treadmill test (target velocity). The pace was gradually increased over the first 5 minutes until reaching the target velocity. The child then trained for 20 minutes and the pace was gradually diminished over the final 5 minutes until the complete halt of the treadmill. Training could be interrupted at any time at the child's request or because of symptoms of fatigue. The physical therapist remained alongside the child throughout the training session. All participants were instructed to maintain their routine therapy (2 weekly sessions of physical therapy following the aforementioned protocol performed in the 8 weeks prior to treadmill training).
The data were analyzed using the Komogorov-Simonov test for the determination of adherence to the Gaussian curve. As parametric distributions were demonstrated, the variables were expressed as mean and standard deviation values. One-way analysis of variance was used for the pretraining and posttraining comparisons of the overall sample (15 children) and the 2 subgroups (group 1—children having undergone soft tissue surgery alone; group 2—children having undergone both soft tissue and bone surgery). The level of significance was set at α < .05. The data were organized and tabulated using the Statistical Package for the Social Sciences (SPSS, v.19.0).
Throughout the study period, 18 children and adolescents who met the eligibility criteria underwent surgery and participated in physical therapy. Two developed postoperative complications (bone consolidation difficulty and pressure ulcer) and 1 family refused to participate in the study. Thus, a total of 15 individuals were included in the present study. Table 1 displays the characteristics of the sample.
The mean number of training sessions throughout the 12-week period was 11.1 ± 1.1 in group 1 and 11.1 ± 0.8 in group 2. No statistically significant differences were found between groups upon the initial evaluation, except with regard to DBP during the 6MWT and treadmill test.
In the overall sample (15 children), significant improvements were found after treadmill training for: GMFM-88 subscale B (before: 90.5 ± 5.7; after: 96.6 ± 4.9; P = .03), subscale C (before: 82.5 ± 17.5; after: 99.2 ± 2.1; P = .01), subscale D (before: 39.4 ± 14.4; after: 75.3 ± 15.2; P = .00), subscale E (before: 30.9 ± 19.4; after: 66.4 ± 19.2; P = .04), and total GMFM-88 score (before: 50.0 ± 17.6; after: 63.3 ± 15.3; P = .05); distance traveled during the 6MWT (before: 166.4 ± 39.1 m; after: 304.7 ± 75.8 m; P = .00); and time tolerated on the treadmill test (before: 5.1 ± 1.1 minutes; after: 15.4 ± 3.5 minutes; P = .00).
In the intragroup analysis, group 1 exhibited significantly higher scores on the posttraining evaluation with regard to GMFM-88 subscales D (P = .00) and E (P = .02) as well as the total GMFM-88 score (P = .05). Group 2 exhibited similar results, with significantly higher scores on the posttraining evaluation with regard to subscales D (P = .00) and E (P = .02) as well as the total score (P = .04) (Table 2). In the intergroup analysis, no statistically significant differences were found between groups with regard to the GMFM-88 scores (subscales and total) following treadmill training.
On the 6MWT, statistically significant differences were found on the posttraining evaluation with regard to HR, RR, SpO2, SBP, DBP, and distance traveled in both groups (Table 3). In the intergroup analysis, group 2 had a significantly higher DBP (P = .03) after the training sessions than group 1.
On the treadmill test used in this study, a statistically significant difference between groups after training was found for DBP alone (P = .00). In the intragroup analysis, statistically significant differences between the pretraining and posttraining evaluations were found with regard to HR, RR, SpO2, SBP, and total time on the treadmill in both groups (Table 4).
Treadmill training is a promising strategy, but the effects of this modality are explored little in the literature. Thus, the aim of this study was to analyze the effect of treadmill training on children with CP having undergone soft tissue surgery (group 1) or both soft tissue and bone surgery (group 2) of the lower limbs.
Functional mobility is an important goal in the rehabilitation process of children with CP. All efforts are made with the intention of facilitating the acquisition and modification of gait, thereby promoting better biomechanical alignment, velocity, and endurance during locomotion. Previous randomized controlled trials have analyzed the effect of treadmill training on gait velocity and endurance using partial body weight support during the training sessions. In studies carried out by Dodd and Foley18 and Willoghby et al,20 functional tests were used to assess velocity (10-m walk test) and endurance (10-Minute Walk Test); the authors reported that gait training with weight support did not lead to an improvement in these parameters. Johnston et al22 studied temporal gait parameters, using a 3-dimensional analysis system, and reported that the group that received treadmill training did not achieve better results than the control group. In the present study, functional mobility was assessed using the 6MWT, which has proven valid for the population studied, and an average improvement of 152.7 and 124.0 m was found in groups 1 and 2, respectively, following treadmill training. The lack of a control group limits comparisons with other studies. According to Thompson et al,27 differences of 64.0 m and 47.4 m on the 6MWT following an intervention are considered clinically significant for children with CP classified at levels II and III of the GMFCS, respectively. In the present study, 13 children demonstrated a clinically significant improvement in the distance traveled (minimum of 70 m and maximum of 240 m farther on the posttraining test) and 2 children traveled 42 m farther after training. The authors believe that the significant increase on the 6MWT and treadmill test were due to both the gait training and the benefits of biomechanical alignment stemming from the surgical procedures. It should be stressed that the sample was only made up of children with functional gait in the preoperative period, unlike the other studies cited, which involved the training of children with more severe functional impairment (GMFCS level IV). Moreover, treadmill training in our study was performed without partial weight support, which differs from the method used in previous investigations involving children with CP.17–22 Further studies should be carried out using partial body weight support in earlier periods of postoperative physical therapy and involving children with GMFCS level IV.
With regard to gross motor function, the results revealed changes in the total GMFM-88 scores of 14.7 and 11.9 in groups 1 and 2, respectively. In studies carried out by Cherng et al17 and Johnston et al,22 GMFM scores improved after gait training on a treadmill with partial body weight support, but the improvement in mean values (4.0 and 2.6, respectively) after training was not as large as in the present investigation. The GMFM-88 scores on the initial evaluation (49.6 in group 1 and 40.3 in group 2) were below the expected values for children with the levels of motor function studied. This was likely due to the period of immobilization, with consequent impairment of motor function, as the final mean scores in both groups (group 1: 64.3 ± 16.2; group 2: 62.7 ± 15.6) were similar to the mean values on the initial evaluation of the experimental and control groups in the studies by Cherng et al17 (65.6 ± 12.5 and 61.5 ± 23.7, respectively) and Johnston et al22 (62.7 ± 17.5 and 58.4 ± 26.9, respectively).
A limitation of this study was the lack of a randomly selected control group of children with CP having undergone orthopedic surgery in the lower limbs without undergoing the gait training program on a treadmill. The control group would have allowed a better evaluation of the results and a more faithful determination of the effect of treadmill training in the critical postoperative period. Moreover, further studies should be carried out with an adequate sample size. Calculating a sample size based on the results of this study, with gross motor function as the main outcome and a bidirectional alpha of .05 and 90% power, a minimum of 18 children would be needed for each group to determine the effect of gait training using a treadmill without body weight support.
The treadmill training program with a frequency of one 30-minute session per week over a 12-week period proved effective in the physical rehabilitation of children with CP having undergone orthopedic surgery in the lower limbs. The treadmill training program leads to an improvement in global gross motor function, especially in the upright position (standing, walking, running, and jumping), and functional mobility. The type of surgery (soft tissue alone or both soft tissue and bone) does not exert an influence on the results of treadmill training.
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adolescent; ambulation; cerebral palsy/rehabilitation; child; exercise therapy/methods; orthopedic surgery/rehabilitation; physical therapy/methods
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