Effect of walking aids and foot orthoses on energy expenditure in children with cerebral palsy: a systematic review

Background Walking aids and ankle–foot orthoses (AFOs) are designed to address gait problems. These devices are common among children with cerebral palsy (CP), as those children’s ability to ambulate is a big concern for their parents, and its improvement is considered primary focus of therapeutic modalities addressing motor disorders of this population. However, empirical support for walking aids and AFO is limited. The aim of this review was to assess the quality of research on the effect of walking aids and AFO on energy expenditure in children with CP. Materials and methods Four electronic databases using predefined terms were searched by two independent reviewers. All study designs except case reports were included. Nineteen studies involving 509 participants met inclusion criteria and were involved in this review. Results Heterogeneity was observed across included studies in measurement, implementation, and study rigor. Conclusion There is a need for high-quality studies to draw a clear conclusion on the effect of walking aids and AFO on energy expenditure in children with CP; the typical flaws of existing studies included weak experimental designs, insubstantial treatment outcomes, and high risk of bias.


Introduction
Cerebral palsy (CP) is a familiar cause of postural and movement disorders among children, which are caused by damage of immature brain. Children with CP have pathological changes of musculoskeletal system. Disorders of balance, muscle tone, and strength are considered primary impairments that are related to central nervous system damage. However, joint deformities and muscle contractures occur in response to musculoskeletal growth and primary impairments and are termed as secondary impairments. All of these impairments allow children with CP to walk with inefficient pattern [1].
Ankle-foot orthoses (AFOs) have been recommended to enhance the dynamic gait efficiency of children with CP [2]. Many authors reported the effectiveness of different types of AFOs on gait kinematics and kinetics [2,3], as well as functional performance, in children with CP [4].
Energy expenditure is the amount of oxygen consumed during physical exertion. The change in energy expenditure during activity reflects the metabolic cost of muscles, from moving the body against gravity and from accelerating and decelerating different body parts [5]. The appropriate use of walking aids improves efficiency, stability, and posture. Walking aids include canes, crutches, and walkers [6].
There is a strong relation between the degree of motor disorders and energy cost of walking [7]. Children with CP often begin their walking later than normal children [8] and walk with a higher energy cost and slower speed [9]. Independent mobility is important for participation, activity, and self-sufficiency, all of which decrease dependence on caregivers. Efficiency and safety are considered essential factors for selecting methods of mobility suited to different environmental conditions [10].
It is essential to measure energy consumption because of its role in the evaluation of functional ability as the quantification of energy expenditure; at the same time, walking provides objective data to assist in the evaluation of children with walking disabilities as well as effectiveness of therapeutic modalities, such as walking aids, orthoses, rehabilitation programmes, and surgical treatments [11].
A previous study performed on AFO and on different types of walkers concluded that high-quality studies are still required to support evidence-based decisions concerning the use of AFOs [12]; low quality of existing evidence and the heterogeneity prevent the recommendation of one walker type over the other, and well-designed studies are needed to provide clinical recommendations [13].
Therefore, there was a need for further research to provide adequate evidence to inform clinical recommendations, with adequately powered studies and careful design to minimize bias.
The purpose of this review was to assess the quality of present research on the effect of walking aids and AFOs on energy expenditure in children with CP.

Literature search
The authors underwent a training programme for online search to be able to perform the searching process in different databases. The following databases were searched to identify relevant published studies: the Cochrane Library, Scopus, PubMed, and the Web of Science. Those databases were searched by using the following keywords: energy expenditure, gait, walking aids, walkers, foot orthosis, CP, diplegia, and hemiplegia. Several search strategies were developed to accommodate the databases.

Study selection and eligibility criteria
Studies were included if they met the following criteria:

Participants
Children with different types of CP of both sex aged up to 18 years old were included. Methodology: studies that investigated the immediate or long-term effect of lower limb orthoses or any type of assisted walking aid on energy expenditure were involved. Study design: all research designs except case reports were accepted.

Language
Full-text papers in English were included.

Data extraction
Two authors (Abd El-Hakiem Abd El-Nabie and Abd El-Aziz) extracted the following items from the included articles: (a) the author and year of publication; (b) information on the population, describing numbers of included children by diagnosis, age, and sex; (c) study design; (d) methodology, including the type of intervention or assessment, technique of its application, and its duration; (e) measured outcomes as explained by their authors; and (f) results. The extracted data are grouped into two tables: Table 1 related to articles that evaluated the effect of orthosis on energy expenditure [14][15][16][17][18][19][20][21][22][23], whereas articles investigating the effect of assisted walking aids, for example, a Walk Aide foot drop stimulator, walkers, sticks, a robotic-assisted gait trainer, and a flexible derotator, on energy expenditure [24][25][26][27][28][29][30][31], were presented in Table 2.

Assessment of methodological quality
Methodological quality in the current systematic review was evaluated by the PEDro scale. This tenitem instrument is a valid measurement of methodological quality of clinical trials. The items are scored as present (1) or absent (0) [32]. Two reviewers (Abd El-Hakiem Abd El-Nabie and Abd El-Aziz) independently assessed the methodological quality of included studies, and discrepancies between them were resolved by consultation with the third author (Elshennawy) to reach the final decision. After each item was classified as 'present' or 'absent', the total score of each study was calculated as the sum of 'present' responses ( Table 3). As reported by Foley et al. [33], the methodological quality was considered to be 'excellent' when studies scored from 9 to 10 on the PEDro scale, whereas studies scoring from 6 to 8 were considered 'good' quality, studies with 4 and 5 scores were graded as 'fair' quality, and studies with a score below 4 were classified as 'poor' quality.

Level of evidence
The level of evidence of all included studies was scored according to the modified Sackett scale (Tables 3 and  4). This five-level scale is used to determine the strength of evidence regarding the intervention (Table 4) [34].

Literature search
The search strategy revealed 981 articles from previously mentioned databases, as follows: Cochrane Library (304), Scopus (70), PubMed (449), and Web of Science (158). Thirty-six duplicated articles out of 981 were found when the results from all databases were combined and screened for duplicate. The reviewers screened titles and abstracts of the remaining 945 articles independently, and the result of this screening was 53 included articles. Fifty-three articles were filtered on the basis of full-text; 34 were excluded because they were outside the scope, because the children's diagnosis was not CP or outcome of interest was absent, or, in one case, the full-text paper was not available, as shown in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow chart (Fig. 1). The remaining 19 studies formed the basis for the current systematic review.

Characteristics of the studies
There was some variability among included studies regarding characteristics of participants (diagnosis and age), study design, methodology, outcome measures, and assessment methods.

Characteristics of participants
The children, who ranged from 3 to 18 years of age, were diagnosed with diplegic, hemiplegic, quadriplegic, and triplegic CP of different levels of severity. Both sexes were represented (261 boys and 173 girls). Two studies, namely, those of El-Shamy et al. [24] and Bhise et al. [14], did not identify sex distributions of their subjects.

Methods
All studies in the current systematic review examined the effect of different types of lower limb orthoses (different configurations of AFO [4,[14][15][16][18][19][20][21][22][23], plastic and metallic knee-AFO [17] or the effect of assisted walking aids (anterior and posterior walkers [27,28,30,31], walking sticks [29], robotic-assisted gait training [25], flexible derotator [26] and Walk Aide foot drop stimulator [24]) on energy expenditure in children with CP. All included studies can be classified into the following types: (a) studies that investigated the immediate effect of lower limb orthoses [14,17,18,20,22,23] or assisted walking aids [28,30,31] on energy expenditure, in which energy expenditure was assessed during the wearing of orthotic devices or during the usage of assisted  With the posterior walker use, there was a reduction in anterior torso tilt and the shoulder extension and elbow flexion were increased Sex: 7 female and 3 male

Upper limb kinematics
Toms et al. [29] Case series walking aids and (b) studies that examined the longterm or cumulative effect of orthoses [4,15,16,19,21] or assisted walking aids [24][25][26]29] on energy expenditure, in which lower limb orthosis or assisted walking aids were applied for a specific duration (weeks or months). In these studies, energy expenditure was evaluated before and after treatment.

Measurement of energy expenditure
Energy expenditure can be measured with different methods. In the present systematic review, all studies were accepted regardless of the method of measuring energy expenditure. Methods of measuring energy expenditure in the included studies were as follows: the energy expenditure index method [17,18,20,26,28] or the Physiological Cost Index method [4,14,23], in which energy expenditure was measured by subtracting the maximum heart rate from the resting heart rate and divided by speed of walking; an open-circuit indirect calorimeter [19,24] or portable breath gas analysis system [15,16,18,22,30,31] which assess energy expenditure by measuring the amount of oxygen consumption; the dilution model [4,21]; and a SenseWear Armband (Table 5) [25]. Table 5 shows methods of measuring energy expenditure in the included studies.

Discussion
Our search in literature revealed moderate-quality to low-quality evidence on the effect of assisted walking aids and foot orthoses on energy expenditure in children with CP. The current systematic review aimed to collect this evidence by using systematic methods for search and evaluating best available studies on the benefit of assisted walking aids and foot orthoses for children with CP, based on clinically relevant outcomes including different methods of measuring energy expenditure, kinematic and kinetic gait parameters, and functional motor skills.
Energy expenditure among children with CP is very important as children with CP consume more energy during ambulation and they have lower physical activity levels and lower energy requirements than do typically developing children [35].
Figueiredo et al. [12] performed a descriptive review of literature about the effect of AFOs on gait in children with CP. They reported that studies with high-quality methods are still desired to support evidence-based decisions on the use of AFOs for those children. As, studies included flaws such as; lack of randomization procedures, lack of parity among groups and no masking of subjects, therapists, and examiners, except for one blinding was mentioned for examiners [12]. Consequently, there has been little progress in the quality of evidence since the last published review on orthoses. Instead of, we found that it is important to address other assisted walking aids used by children with CP to clarify its effect on energy expenditure because they were not addressed in any other systematic reviews. It should be borne in mind that ambulation with assisted walking aids is incorporated into daily life, so energy conservation is a major issue when choosing walking aids [30].
Different mechanisms have been suggested to clarify the advantage of foot orthoses for children with CP; one of them is the improvement of energy expenditure after using foot orthoses. Because the use of foot orthoses results in normal ankle motion during stance phase, this might lead to increased stability, with decreases in mechanical power and reduction in O 2 cost of walking [36].
Another explanation mentioned when using other assisted walking aids like walkers revealed that posterior walker gives children with CP more stability as it decreases flexion angles of trunk, hips, and knees and gives more upright posture for them [37].
This review analyzed 19 studies; most of them were a cross-sectional design. This design enables researchers to estimate the prevalence of increased energy expenditure in children with CP and gave the best opportunities to know the different treatment modalities used to improve it. Studies with crosssectional design provide a 'snapshot' of characteristics and outcomes associated with it, at a specific time [35] . Results of all included studies in this systematic review were consistent and agreed that foot orthoses and other assisted walking aids may improve energy expenditure in children with CP.
This review found moderate-quality to low-quality evidence supporting the use of foot orthoses and other assisted walking aids for children with CP; it also highlighted the variation in use of assisted walking aids and foot orthoses (types, duration, and technique of application), outcomes, and follow-up in the Strifling et al. [28] Energy expenditure index method Brehm et al. [18] Oxygen consumption measured by breathby-breath gas analysis Konop et al. [27] Energy expenditure index method Kerkum et al. [16] Oxygen uptake measured by a portable breath gas analysis system Toms et al. [29] Physiological Cost Index included studies. This clinical heterogeneity (characteristic of participants, absence of allocation concealment and blinding, small sample sizes, and wide variability) restricted the comparison between results of these studies and made meta-analysis inapplicable.
According to this results of PEDro scale, we had only two studies with moderate methodological quality and 17 studies with low quality. This might be owing to the absence of blindness in studies, which may be affected by the type of intervention used.

Conclusion
Results of the current review revealed moderate-quality to low-quality evidence, and they were consistent and agreed that foot orthoses and assisted walking aids can improve energy expenditure in children with CP.

Recommendation
Well-designed and high-quality studies on the effect of foot orthoses and assisted walking aids on energy expenditure in children with CP are still needed to provide strong evidence.