Treadmill training as a form of rehabilitation in children and adolescents with cerebral palsy: a literature review
Jakub Gąsior, Mariusz Pawłowski, Piotr Jeleń, Marcin Bonikowski, Janusz Błaszczyk
The aim of this article was to review the existing literature on the effectiveness and safety of treadmill training in children and adolescents with cerebral palsy (CP). Medical databases were searched using the keyword sequence: cerebral palsy and treadmill training. Of 23 search results, 17 publications met our inclusion criteria. The literature review outcomes are presented according to the International Classification of Functioning, Disability and Health at three levels: structure, activity and participation. The studies indicate that treadmill training in children and adolescents with CP may be effective. Statistical significance was demonstrated in 12 out of 17 studies. The authors reported improvement in gait parameters and in the quality of life of the patients undergoing the treadmill training. No side effects were observed. The analyzed studies differed in the treadmill training methodology as well as in patient groups – volunteers undergoing the training exhibited various severities of symptoms. It still remains necessary to determine the characteristics of patients who could benefit the most and to develop individually-designed training protocols, which would allow maximum therapeutic benefit to be achieved from the treadmill training.
Cerebral palsy (CP) is a group of movement and posture disorders resulting from damage to the central nervous system (CNS) in the fetal or early postnatal periods. Although damage to the CNS in CP is non-progressive [1, 2], the symptoms may intensify. Symptoms of CP are generally classified as positive (redundant) or negative. Positive symptoms are defined as those which lead to an increase in involuntary muscle activity, range of motion or amount of movement patterns, examples being chorea, tics, tremor and hypertonia caused by spasticity, rigidity or dystonia. Negative symptoms include inadequate or insufficient control of muscle activity, such as muscle weakness, loss of selective motor control, ataxia or dyspraxia [3, 4]. Positive and negative symptoms usually occur simultaneously and over time, can lead to abnormal gait , which is observed in about 90% of patients with CP . In Mazovia Province, Poland, the incidence of CP in children born before 32 weeks of gestation is 8%. At the age of about 6 years, 60% of these children require assistance in moving . The ability to walk independently allows a patient with CP to participate more fully in daily activities and relationships with peers , and so one of the main objectives of rehabilitation for these patients is to achieve an independent, efficient gait and /or improve the gait pattern .
Despite advances in Medicine, to date there is no possibility to cure patients with CP. However in this group of disorders, the emphasis is put on the development of methods to improve the condition of the patient, i.e. symptomatic treatment and rehabilitation . These methods are primarily focused on achieving the improvement in the function of the musculo-skeletal and neuromuscular system. They include pharmacological treatment (i.e. botulinum toxin), neurosurgery (i.e. selective dorsal rhizotomy), orthopaedic treatment (i.e. tendotomy, miotomy, corrective osteotomy) and rehabilitation with orthopaedic appliances. All of these procedures are designed to improve the independent mobility of the patient .
One way to improve the condition of patients with damage to the CNS, aimed at improving locomotion, is a workout on a treadmill with or without body weight support [11, 12]. The results of previous studies conducted on animal models show that this type of training may contribute to improvements in nervous system plasticity processes , extensions in the surface area (soma) of the motor neurons , or may increase the cross-sectional area of muscle fibres . Furthermore it has been shown that a walk on the treadmill stimulates the activity of neuronal circuits within the spinal cord involved in generating locomotor movement, thus allowing a formation of rhythmic, automatic movement patterns [16–18].
English language literature includes many reports on the effectiveness of treadmill training in children and adolescents with CP. This topic has not been previously addressed by Polish literature, which tends to be dedicated to a broader physiotherapy environment. The aim of this study is to present the issue of the treadmill training and to determine whether it can be effective and safe in patients with CP, based on a review of world literature.
As contemporary neurorehabilitation should implement therapies in accordance with the rules of Evidence Based Medicine (EBM) in daily practice, the chosen method of rehabilitation should be based on thoroughly researched methods [19, 20]. Therefore, to identify the level of scientific evidence, the results included in this review were evaluated according to the Sackett scale . The assessment of the level of scientific evidence depends on the type of research project. The first, highest, level of the scale refers to randomized trials, the second refers to the prospective controlled trials and cohort studies. Level 3 includes case control trials, level 4 includes testing pre-post studies and case series/clinical series, while Level 5 refers to observational studies, developed clinical consensus and case reports .
The results were presented according to the structure of the International Classification of Functioning, Disability and Health [22–24], which proposes describing patient functioning in relation to the structure of the human body, human activity as a unit, and the participation of the patient in everyday life .
Materials and Methods
Medical databases such as CINAHL, PubMed, EMBASE, and the Cochrane Library were searched using the keyword “cerebral palsy’ together with “treadmill training”, “body weight supported treadmill training” or “partial body weight supported treadmill training”. All kinds of research projects were analysed. Besides the occurrence of keywords, the following inclusion criteria were also applied: publication date from January 1997 to November 2013, age of participants below 18 years of age.
Although the aim of this study was to evaluate the efficacy of treadmill training in the rehabilitation of patients with CP, studies comparing different types of training, for example, treadmill training with gait training on a stationary surface (fixed, flat, horizontal surface) or studies comparing training with support and trainings without support, were included in the Discussion part. Publications comparing treadmill training with another form of treatment were excluded.
The variety of research methods in relation to the patient (functional level measured by the Gross Motor Function Classification System – GMFCS), diverse interventions (type and percentage of body relief, the treadmill speed, the duration of training), different ways to measure outcomes (research tools) and the quality of research (Sackett's scale) did not allow a quantitative analysis, a meta-analysis, to be performed.After the graphic symbol, in brackets, the percentage values of increase or decrease of the tested variable were placed.
Some studies (Richards et al. , McNevin et al. , Day et al. , Dieruf et al. , Kurz et al. ) present the results of different variables or the results of particular patients in a graphic form. In these articles, the researchers do not consider the statistical significance of the results. To improve the readability of the results of the analysed publications, the results of the reviewed papers are presented in Table I in graphic form (↑, ↓ or -) and show a percentage change where possible. In addition, detailed, statistically significant results are discussed in the Results part of the literature review. This graphical form of presentation was adapted from a review article published in the Journal of Rehabilitation Medicine .. In order to determine common abbreviations which appear in the text and require clarification or augmentation, a key is given in the subscript of the table.
Summary of the literature review
Twenty-three publications were identified during the database search, including three review papers [32–34]. Two articles [35, 36] did not have full access and one article comparing treadmill training with strength training  was rejected. Finally, 17 publications that met the inclusion criteria for the review were analysed (Table I).
Three works were assessed at level 1B, twelve at level 2B and two at level 4 according to the Sackett scale.
Characteristics of the experimental groups
In total, 159 patients were recruited in the chosen studies describing treadmill training in children and adolescents with CP, including 33 diagnosed with diplegia, 6 with hemiplegia, 24 with tetraplegia and 6 with hypotonia. In five articles, the type of CP was not specified (“participants’ characteristics”, Table 1). Patients participating in the study were evaluated at all levels (I–V) according to the GMFCS (Gross Motor Function Classification System). The mean age of the experimental groups was 9.1 years (SD 4.4 years). The youngest patient was 15 months of age , the oldest was 18 years .
Methodology of treadmill training
A detailed description of the training methodology is shown in the Table I, in the column called "Therapeutic intervention". According to the reviewed articles, training on the treadmill lasted on average 8 weeks (2–25, usually 6), with an average frequency of 4 times per week (2–12, usually 2). Body weight support was used in 12 studies and the majority used corsets. One study used lower body positive pressure supported treadmill training (LBPPSTT) . In the majority of articles, the body weight support was progressively weaned away during the training. The highest percentage of body unloading was 60% . Three studies did not apply body weight support.
As walking speed on the treadmill was measured in different units (m/s, cm/s, km/h, mph), Table 1 ("Results" column) shows their equivalents as SI units (m/s) in brackets, in addition to the data specified in the original units. In 14 studies, physical therapists or parents helped to normalise and/or stabilise the patient's gait. In order to increase motivation and/or co-operation with the patient, four studies used a mirror placed in front of the treadmill, or toys and games. In eight studies, apart from the training on a treadmill, patients were subjected to regular physiotherapy. In seven studies, patients used orthoses during exercise on a treadmill. Treadmill workouts were performed individually at home, at school or in a rehabilitation centre.
ResultsThe following ICF classification levels were taken into account when assessing the results of treadmill training presented in the analysed publications: structure, activity and participation. In the papers found in the medical databases only the statistically significant results were discussed in detail.
ICF Level - structure
Two publications assessed the impact of treadmill training on muscle strength. The studies report that the strength of the antigravity muscles increased by 24% in total . One study assessed the H-reflex (Hoffmann's reflex) of the soleus muscle during walking on a treadmill without body weight support. To allow comparison between patients, the size of H-reflex was standardised and expressed as a percentage of the maximum response amplitude M (% Mmax). After 10 days of training, the average H-wave amplitude decreased during the full phase of the full gait cycle as well as the swing phase by 14.1% Mmax and 11.8% Mmax, respectively .
ICF Level: Activity
In order to document changes in gross motor function observed after a workout on a treadmill, a scale for assessing gross motor function (GMFM – Gross Motor Function Measure) was used [26, 28, 38, 39, 42–46]. Significant changes were observed in four of the nine studies. The experimental group showed a significant increase in the scores of the GMFM-88 full scale from 82% to 93%, and in its dimensions: C (crawling and kneeing): from 88% to 96% , D (standing) from 11 to 16 points , from 61% to 84%  and E (walking, running, jumping) from 10 to 14 scores , from 72% to 92% . The experimental group obtained higher performance results when compared with the control group (overground walking) on the GMFM-88 scale (11% vs. 4%), C dimensions (8% vs. 2%), D (24% vs. 8 %) and E (20% vs. 8%) . The other two studies [38, 45] show the results in graphical form, making it impossible to provide specific outcomes.
For a comprehensive assessment of changes in the patient's functional abilities, the Paediatric Evaluation of Disability Inventory (PEDI) scale was used [28, 38, 43, 45, 46]. Significant changes were observed in two of the five studies [38, 46]. The experimental group demonstrated an increase in the values of an overall assessment (from 128 to 139 points) as well as on a scale of mobility (from 33 to 44.9 points) and on a scale of social functions (from 52.2 to 53 points). An increase in the overall assessment values (11 vs. 4 points of growth) and the mobility scale (11.9 vs. 3.7 points increase) was observed when compared with the control group .
Fourteen studies examined the selected parameters of gait after a workout on the treadmill. Changes were observed in six studies [40–42, 45–47]. When performing a 10-minute walk test (10 MWT) the experimental group showed an increase in speed by 0.19 m/s , 0.07 m/s  and 0.02 m/s . The experimental group also demonstrated an increase in the speed on the treadmill by 0.47 m/s , 0.24 m/s  and 0.17 m/s  accordingly. Distance travelled was measured using walk tests of 6 or 10 minutes in duration (6 -, 10-MWT) [30, 42, 45–48] or electronically on a treadmill [45, 48]. The experimental group demonstrated an increase in distance travelled (149.8m) assessed by 6MWT. After the tests on the treadmill, the experimental group demonstrated increases in walking distance of 420.8 m  and 105.5 m . Walking time was evaluated on both over-ground walking  and on the treadmill [45, 46, 48]. A prolongation of walking time on a treadmill in the experimental group by 7.1 min , 3.3 min  and 3.2 min  was observed.
Analyzing the other variables in the dimension of activity, a decrease in the difference of step length between the lower limbs of 2.7 cm , a reduction in Energy Expenditure Index (EEI) of 0.29 heart beats per minute , an increased duration of the transmission phase (2.5% of the step time), reduction in duration of the stance phase (2.3% of each step) , reduction in duration of the double stance phase by 0.17 s , and reduction of heart rate by 38.4 beats per minute  were observed.
Training on a treadmill conducted in an inflatable bag using air pressure to support the child’s weight (LBPPSTT) contributed to the improvement of balance assessed in the BESTest test. Among the patients of the experimental group, assessed according to the GMFCS scale at level II-III, improvements from 71 to 82 points  were observed. In the other two studies, no significant changes were noted [44, 45].
The influence of training on the treadmill for functional stability (Berg balance scale) and static stability (Stabilographic platform) was assessed. Functional (from 34.9 to 46.7 points) and static improvements were observed. The reduction in average deflections was expressed in the experimental group in the sagittal plane (from 1.4 cm to 1.0 cm) and in the coronal plane (-1.2 cm vs. 0.3 cm)  when compared with the control group.
Two studies compared the physiological cost of walking on a treadmill with a body weight support to a gait without support (oxygen consumption, ventilation, heart rate ; heart rate, blood pressure, fatigue ). During the exercise with unloading of 30% of the patient's body, lower heart rate, decreased systolic and diastolic blood pressure and a lower degree of fatigue (Borg scale) were achieved when compared with unbalanced gait . In the group of five children with spastic diplegia it was proven that a 4-minute walk on a treadmill with unloading (8-52% of body weight) has a lower relative (difference of 3.7 ml x kg-1 x min-1) and total (difference of 153.5 ml/min) oxygen consumption and smaller pulmonary ventilation (a difference of 3.2 L/min)  when compared with unbalanced gait.
In addition to time-distance, corridor gait tests and evaluation on a GMFM scale, mobility was also assessed using other tests and scales (Table I). A 42% improvement on a scale of independent, functional gait - FAC (called Functional Ambulation Categories)  was reported in the experimental group compared with the control group, as well as a 6.5s reduction in duration of a timed up and go test (TUG) , an improvement in the Peabody Developmental Motor Scales-2 (PDMS-2) and Functional Mobility Scale (FMS) .
ICF level: participation in everyday life/quality of life
The influence of treadmill training on the quality of life of the child and the parent / guardian was assessed. Using the Peds QL questionnaire, a significant improvement in overall quality of life in a group of 4 children and 4 parents/guardians was noted. Also the improvement in physical functioning sections (4 parents/guardians, 1 child) and psychosocial (2 parents/ guardians, 4 children) were reported. The study did not evaluate the level of statistical significance of the effects .
Long-term evaluation of the effects
Four of the seventeen studies evaluated the long-term effects of training on the treadmill [38, 45, 46, 48]. To obtain this, an assessment was made 6.5 weeks after the cessation of the treadmill training (4–16, usually 4 weeks).
According to Mattern-Baxter et al. [38, 45] four weeks after the end of the 4-week treadmill training period, the time required to walk 10 meters decreased and the distance travelled during the 6 minute walk increased. The results reached statistical significance in post-hoc tests. The authors presented the outcomes in graphical form, making it impossible to provide detailed numerical results.
Tests on a treadmill showed that the walking distance and the time of walking decreased and were successively 122.2 m (151.8 m immediately after workout), 492.2 s (564.5 s immediately after workout) and the speed increased and reached a value of 0.3 m/s (0.25 m/s immediately after training). The functional abilities of patients on the PEDI scale reached statistical significance. The authors of another study evaluated the results 4- and 16-weeks after the 6-week training on the treadmill . The statistical significance – when compared with the results obtained immediately after the training – was achieved in the values of gross motor expressed in dimensions D and E of the GMFM scale, PDMS-2, PEDI, 10MWT, FMS and the number of steps taken during 10s.
Grecco et al.  note that the values of the results obtained 4 weeks after the 7-week treadmill training period decreased, but remained statistically significant when compared with the results obtained before the training. The result of the 6MWT distance was 360.2 m (directly after the training 377.2 m), walking time on the treadmill was 8.9 min (9.8 min after training), and walking speed on the treadmill was 4.2 km/h (after training 4.9 km/h). Patient mobility and social function results according to the PEDI scale were 43.8 points (after training 44.9) and 52.8 points (after training 53). Patients score on a GMFM-88 scale was 91.7 (after training 93) and in its dimensions: D – score 82.4 (after training 84.4) and E - score 91.8 (after training 92.3). The functional stability was assessed as score 46.2 (after training 46.7). On the assessment some values increased: TUG test time was 8.6 s (7.8 s after exercise), heart rate reached 118 beats/min (after training 117) and the overall PEDI scale score was 140.8 points (after Training 139).
The safety of treadmill training
None of the included studies reported any negative side effects to treadmill training.
Increasing interest in the use of treadmill training can be found in Anglophonic scientific literature, both with and without body weight support, in the treatment of patients with CP, which is demonstrated by the steadily growing number of publications devoted to this topic. However, so far this subject has not been of interest to Polish specialist journals. The purpose of this paper was to introduce the topic of the therapeutic use of treadmill training to the current body of Polish research literature pertaining to Physiotherapy and the neuro-rehabilitation of children and adolescents with CP. Moreover, another aim of the review is to summarise findings concerning whether this type of therapy is effective and safe, and when it should be used.
Comprehensive rehabilitation plays an important role in the treatment of patients with CP, with high intensity, frequency, and the use of various techniques being recommended to improve the condition of the patient . The contemporary model of rehabilitation focused on the task (motor learning theory, functional therapy) emphasizes that early implemented, intensive, frequently repeated practice of the specific task, with the active participation of the patient, is crucial for the recovery of motor skills after brain injury [50–53]. The therapist can incorporate all of these components in the process of rehabilitation of patients with CP by using treadmill training.
Of the reviewed studies conducted on groups of adolescents with CP, best results at the level of gross motor function (activity) were achieved in studies with a longer duration of training (12 and 7 weeks) [39,46]. The mean age of the patients was 11-12 years and 6-7 years respectively, which suggests that the results achieved are effects of the physiotherapy intervention and not those of puberty of the patients . In Grecco et al. , the training took place without body weight support. Among patients evaluated at the level of GMFCS I-III (independent gait), an improvement in gross motor assessment scales GMFM and functional capabilities (PEDI) resulted in improved mobility – increased distance, time and speed of walking, and better stability - reduced deflections in the sagittal and coronal planes: a randomized study with a control group, which was subjected to gait training on a stationary surface. A methodologically similar study conducted by Willoughby et al. , evaluated patients aged 10 years, but not moving independently (GMFCS III–IV) during training with unloading lasting 9 weeks. An improvement in the walking distance and time on the treadmill was obtained without improvement in waking speed on a stationary surface. In Dodd et al. , where the experimental group was also evaluated according to the GMFCS level III–IV, an improvement of walking speed after a 6-week-long training on the treadmill was observed when compared with the control group with no training on the treadmill. Grecco et al. , Dodd et al.  and Willoughby et al.  obtained the highest score amongst the existing research, reaching level 1B on the Sackett's scale.
Among the studies with the lowest level of scientific evidence, the study of Phillips et al. , conducted among teenagers at the age of 10, walking independently (GMFCS I), shows that an intensive two-week training on a treadmill with decreasing unloading increases the activity of the CNS leading to increased plasticity, improved speed  and higher energy consumption during walking , which influences the quality of life of the patient and the parent . Kurz et al.  used a positive pressure inflatable bag supporting 40% of patient’s body weight. After a 6-week training period, patients (GMFCS II–IV) with a mean age of 13 years increased the overall strength of the antigravity muscles, improved balance, and increased walking speed. The results of the above-mentioned studies show that among adolescents with CP, both long-term and short-term intensive training on the treadmill can have positive results expressed by improved mobility.
All studies based on children under the age of 5 were assessed at level 2B by Sackett’s scale. One of the first studies in the history, evaluating the treadmill training in CP patients, was conducted by Richards et al. in 1997 . The experimental group consisted of patients aged 2 years moving non-independently. After the 16-week training period, an 8 to 23% improvement in gross motor was observed, as well as an improvement in the walking speed and gait efficiency with orthopaedic aids, according to SWAPS (Supported Walker Ambulation Performance Scale). Mattern-Baxter et al.  conducted supported training based on patients with an average age of 3 years (GMFCS I-IV) and who were not independent walkers.
Statistically sgnificant results were achieved in the tests conducted immediately after a 4-week training exercise on the treadmill, and improved speed, increased distance and time of walking were observed. The long-term effect was assessed one month after the end of training and significant improvements were observed in the motor activity (PEDI and GMFM) and corridor walk tests. In the second study of this author the experimental group were young children (15,5-32 months) walking independently (GMFCS I-II). Training on a treadmill took place at home without any body weight support. Most of the positive results were observed when assessing the long-term effects one and four months after the end of training. There was a significant improvement in gross motor function (GMFM-66, PEDI) and mobility (PDMS-2, FMS, 10MWT). These three studies show that training on a treadmill with and without support in children under the age of 5, independent and non-independent walkers, may have positive results. In addition, it is believed that training on a treadmill implemented early, together with growing up and puberty can accelerate the achievement of the milestones in child development .
The authors of the reviews included in this study suggest that treadmill training can be effective in children and adolescents with CP. Due to the low level of scientific evidence, and the above mentioned differences between studies, the emphasis is put on the need to conduct randomized studies on a larger group of patients with CP . Moreover, because of the accessibility of equipment such as treadmills, it is recommended to carry out research in many centres, without implementation of additional forms of therapy [32, 33]. Finally, it is suggested that the future studies should involve an assessment of the impact the training exerts on participation of patients in everyday life, according to the ICF . In 2013, a comprehensive review of therapeutic interventions in patients with CP highlighted the need for further research and increase in the level of scientific proof for the effectiveness of treadmill training in this group of patients .
This literature review indicates the possibility to achieve positive but differentiated therapeutic effects resulting from the use of treadmill training for children and adolescents with CP. This is probably due to different inclusion criteria for the study: a large range of patient ages and GMFCS levels, or the time elapsed since the last surgery and/or pharmacological treatment. It is necessary to determine a complete characterization of patients with CP, that would meet the minimum requirements for training on the treadmill and the proper training protocol, which, together, would allow maximum therapeutic benefit to be achieved.
A detailed diagnosis of the functional capabilities of the child and identification of the most vulnerable groups of muscles, spasticity or existing fixed contractures are necessary to achieve this aim. It should be noted that there are many potential contextual factors that may have an significant impact on the effectiveness of the therapy: the right motivation, emotional and intellectual efficiency of the child and establishment of clear objectives consistent to the patient, parent and the therapeutic team being some of them.
The results of the latest research on animal models with CP are optimistic. They suggest a beneficial effect of training on a treadmill in connection with the injection of botulinum toxin type A [56, 57]. There are, however, no reports of previous use of this method in humans.
Future studies need to clarify the following issues: What group of patients with CP (age, GMFCS level) should participate in training on the treadmill to reach the maximum of its therapeutic benefits? Whether, and if so, what contextual factors should be considered in patients with CP, when applying treadmill rehabilitation? And finally, could treadmill exercise provide better results in combination with another form of therapy such as a botulinum toxin injection? The authors hope that this literature review will provide therapeutic teams involved in the treatment and rehabilitation of patients with MPD sufficient arguments for the incorporation of treadmill training into rehabilitation methods used so far.
The review of current literature clearly shows that treadmill training improves physical activity in children and adolescents with CP. No study reported any negative effect to be associated with of this type of training. Particularly marked improvement was observed on the levels of activity and quality of life. The variety of experimental procedures and treatment groups of patients eligible for the training hindered the comparison of the effects of the results obtained by various research groups. There is a need to intensify research in this area increasing the number of patients in the study group, selecting an appropriate control group and using comparative research and therapeutic procedures. Apart from assessing the level of scientific evidence for justification of the conclusions drawn from the results of research, it is also important to adopt a research methodology which will allow an evaluation of their reliability and reproducibility, which is already in the planning stage.
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Jason Roberts, Eduardo Savine Mayr, Dominik Rymer, Bartosz Zielski