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Effectiveness of resistance strength training in children and adolescents with ≥30% total body surface area: A systematic review

Purpose Children and adolescents with burn injuries are at risk of living with social, educational, physical and psychological impairments. The systematic review aimed to ascertain the effectiveness of resistance strength training on muscle strength and lean body mass (LBM) in children and adolescents with burn injuries. Method Five databases were searched. Randomised controlled trials with an intervention defined as a supervised, individualised resistance exercise programme were sought. The outcomes included muscle strength and/or LBM. The PEDro scale was used to describe the methodological quality. Comparable data were combined using RevMan©. Results Seven papers were included in the review with an average methodological appraisal score of 5.7/11. Comparable data were combined for muscle strength and LBM. The meta-analysis revealed no significant clinical difference between the exercise and standard care groups after 3 months of strength training for both muscle strength (p = 0.43) and LBM (p = 0.60). Conclusions There is no conclusive evidence to support the benefit of strength training for children and adolescents with burns injuries in terms of muscle strength and LBM. However, it appears that isokinetic training might benefit children and adolescents with burns, but more studies investigating the effect of isokinetic training are required.

Introduction appearance and functionality. Physiotherapy management includes respiratory management, oedema control, stretching and strengthening exercises as well as splints to maintain the achieved range of movement (ROM) and for contracture prevention (Simons, King & Edgar 2003). Scar management includes compression and massaging techniques for the optimal formation of a functional scar. Aerobic exercise is an important element of physiotherapy management to improve exercise tolerance and cardiovascular endurance (Disseldorp et al. 2011). Physiotherapy is applied in various phases of burn rehabilitation because of the extensive physiological complications.
The inflammatory response after a burn injury triggers a hypermetabolic reaction. This is characterised by a hyperdynamic reaction with increased body temperature, oxygen and glucose consumption, CO 2 production, glycogenolysis, proteolysis, lipolysis and futile substrate cycling (Jeschke et al. 2008). This hypermetabolic response continues up to 24 months post-burn, causing loss of lean body mass (LBM), bone density and muscle weakness (Atiyeh, Gunn & Dibo 2008;Esselman et al. 2006). Considering these cascade of events and the effect on muscle strength, it seems worthwhile for physiotherapists to consider resistance exercises as a strengthening modality for children and adolescents with burns.
The primary aim of resistance exercises is to improve muscle strength. Training close to the muscle's force-generating capacity increases muscle tension, which initiates skeletal muscle growth, therefore affecting LBM (Grisbrook et al. 2013). Resistance training causes an acceleration of protein synthesis on cellular level by predominantly increasing the amount of contractile proteins, thus leading to muscle hypertrophy, which improves muscle size and force output (Grisbrook et al. 2013;Phillips et al. 1999). Disseldorp et al. (2011) conducted a review to assess the effect of progressive resistance exercise (PRE) training on physical fitness of burn patients of all ages. The findings were synthesised descriptively, and they proposed that exercise training improves muscular strength, muscular and cardiorespiratory endurance, body composition and flexibility in children and adolescents. However, a meta-analysis was not conducted and sample sizes were small and not justified. Therefore, it remains unclear whether there is high level evidence to recommend PRE to clinicians. In addition, since the review by Disseldorp et al. (2011), more studies have been published.
The aim of this systematic review was to ascertain the effectiveness of the combination of an individualised, supervised strengthening programme (resistance exercises) with standard care to standard care alone, on muscle strength and LBM in children and adolescents with burn injuries >30% total body surface area (TBSA). The cut off of >30% TBSA was chosen as Baker et al. (2007) reported that an important long-term consequence of paediatric burns >30% TBSA was general muscle weakness affecting the function of young adults and the authors stressed that more emphasis should be placed on strengthening during the rehabilitation phase. Using meta-analytical analyses to increase statistical power of the treatment effect, clinical recommendations can then be based on the current evidence base.

Search strategy
Five databases (CINAHL, Cochrane Library, PubMed, ScienceDirect and Scopus) were searched from inception to September 2015. The search was performed independently by two research groups (H.B., E.C., C.A.G., C.L. and Y.B., Q.L.), using the following key search terms: exercise, lean body mass, muscle strength, burns, thermal injuries, children and adolescents. The two research groups independently screened the titles and abstracts, thereafter potential full text papers were obtained and evaluated according to the inclusion and exclusion criteria.

Inclusion criteria
Randomised controlled trials, published in English and available in full text, were included. There was no limitation in the range of publication date, and papers published up until September 2015 were included. Both male and female children and adolescents (6-18 years) with greater than 30% TBSA were the participants in the trials. The intervention was defined as a supervised, individualised (patient specific) resistance exercise programme of the upper and/or lower limbs in combination with standard care, which commenced within 1 year of the injury and continued for at least 12 weeks. The control group only received standard care consisting of burn wound medication, physiotherapy, wound care, psychological care, nutritional care and occupational therapy. The eligible papers must have reported on both muscle strength and/or LBM post-intervention. Muscle strength could be measured using a dynamometer; the 3 repetition maximum (3RM) technique or any other valid objective instrument. LBM could be measured with dual-energy X-ray absorptiometry (DEXA) or any other valid objective instrument.

Exclusion criteria
Papers including participants with (1) leg amputation, (2) psychological disorders, (3) quadriplegia, (4) severe cognitive disorders, (5) developmental delay before hospitalisation, (6) neurological injury, (7) previously sustained significant hearing/vision loss and (8) post-burn injuries of more than 1 year were excluded from the review. The exclusion criteria include patients who would have been physically and/or mentally unable to complete the intervention programme over and above standard care procedures.

Methodological appraisal
The PEDro scale was used to describe the methodological quality of the eligible studies. The PEDro score is based on the Delphi list and scales 11 items (Table 1). Items are scored as either present (1) or absent (0), and a score out of 11 is calculated by summation (De Morton 2009). Each paper was scored, and discrepancies were discussed in order to reach consensus. The scores from the PEDro scale are not indicative of the effectiveness or the clinical relevance of the studies (Verhagen et al. 1998).

Data extraction and analysis
The adapted Joanna Briggs Institute Data Extraction Form was used to extract data from the papers under the following subheadings: citation, study type, participants, interventions (treatment and control group), outcome measures, results and the clinical status post-intervention and clinical implication thereof (Godfrey & Harrison 2012). When additional data were required, the authors were contacted in order to complete the data extraction process.
The comparable, homogenous data within individual studies, such as patient populations, interventions and outcome measures, were combined using the RevMan© Review Manager Software (RevMan© 2014). This metaanalysis allowed the interpretation of the effectiveness of the combination of a supervised strengthening exercise programme with standard care compared to standard care alone.

Methodological appraisal
The average methodological appraisal score was 5.7 out of 11. Two studies scored 4 (Hardee et al. 2014;, one study scored 5 (Suman et al. 2001), three studies scored 6 (Al- Mousawi et al. 2010;Cucuzzo et al. 2001;Przkora et al. 2007) and one study scored 9 (Ebid et al. 2014). None of the studies met the following two criteria on the PEDro scale: (5) blinding of subjects and (6) blinding of therapists (Table 1)

Study samples
The seven eligible studies varied in sample size, ranging from 19 to 47 participants. The mean age was similar across studies ranging from 9.2 to 13.7 years (the SD was not reported in all studies), although both exercise and standard care groups favoured more male than female to the criteria; x = non-adherence to the criteria. Item 1: specified eligibility criteria; Item 2: random allocation; Item 3: concealed allocation; Item 4: similarity at baseline; Item 5: subject blinding; Item 6: therapist blinding; Item 7: assessor blinding; Item 8: >85% follow-up for at least one outcome; Item 9: intention-to-treat analysis; Item 10: between-group statistical comparison for at least one key outcome, and Item 11: end point and variability measures for at least one key outcome.
Source: Authors' own work FIGURE 1: Results of the search strategy.   (Table 3). Six studies included participants with ≥ 40% TBSA, and one study by Ebid et al. (2014) included participants with ≥ 36% TBSA. All the studies except one (Ebid et al. 2014) were conducted at the same institution in the United States.

Study interventions
All seven interventions were hospital-based individualised and supervised exercise programmes (Table 4) The interventions persisted for 12 weeks post-baseline assessment. The standard care, which was continued from hospital discharge and persisted for the duration of the intervention, included conventional physiotherapy and occupational therapy without individualisation or supervision of exercises. All standard care programmes were home-based except for Hardee et al. (2014), who implemented a hospital-based programme (Table 4).

Effect of a resistance exercise programme on muscle strength and LBM in children and adolescents with burns
Two studies could not be included in the meta-analysis because Cucuzzo et al. (2001) and Hardee et al. (2014) did not report the post-intervention point and variability measures (mean and SD) of muscle strength and LBM, respectively, and the authors did not respond to email communication. The comparable data (means and SD) for the outcome muscle strength were combined from five studies (Al-Mousawi et al. 2010;Ebid et al. 2014;Przkora et al. 2007;Suman et al. 2001; and the metaanalysis revealed that there is no clinically significant difference between the exercise and standard care groups after 3 months of individualised supervised resistance strength training (p = 0.43). Heterogeneity in the summary effect of the combined studies was significantly (p = 0.001) high (78%) (Figure 2). This could be because of clinical differences between the studies in terms of the type of resistance training and the time interval post-burn injury when the intervention commenced. Ebid et al. (2014) included isokinetic resistance exercises and commenced with the intervention 1 month post-burn, whereas the other four studies implemented PREs as the intervention and commenced 6 months post-burn injury (Al-Mousawi et al. 2010;Przkora et al. 2007;Suman et al. 2001;.

Muscle strength
Methodological differences between the studies could also explain the high level of heterogeneity since Ebid et al. (2014) scored 9 and the other four studies (Al-Mousawi et al. 2010;Przkora et al. 2007;Suman et al. 2001; scored between 4 and 6 out of 11 on the PEDro scale. Furthermore, Ebid et al. (2014), whose study had the greatest weighted percentage effect on the summary estimate, could also be seen as an outlier, thus increasing the heterogeneity. Therefore Ebid et al. (2014) and the other four studies (Al-Mousawi et al. 2010;Przkora et al. 2007;Suman et al. 2001; were analysed separately and the forest plots are presented in Figures 3 and 4. The estimated treatment effect of isokinetic strength training showed a significant clinical effect (p <0.00001) favouring the exercise group compared to standard care alone.
Although the combined effect of the studies implementing PRE indicated no heterogeneity between the studies, the summary estimate of the average effect of PRE on muscle strength revealed that there is no clinically significant difference between the exercise and the standard care groups (p = 0.94). (2007) also reported a significant increase in mean percentage change for muscle strength in both the exercise (17.9%) and standard care (7.2%) groups at 1 year post-burn; however, neither increase were significant.

FIGURE 2:
A forest plot to show the summary estimate of the average effect of resistance strengthening exercises on muscle strength at 3 months post-intervention.

Discussion
This systematic review analysed the effect of a 12-week resistance strengthening exercise programme in addition to standard care compared to standard care alone, when managing children or adolescents with burns. The metaanalysis indicated no added benefit for muscle strength and LBM because of strength training when the intervention is implemented within 1-6 months post-injury.
The lack of a clinical difference in muscle strength postintervention between the exercise and standard care groups could be because of the difference in baseline muscle strength values between the two groups ( Table 2). The two studies (Ebid et al. 2014;Przkora et al. 2007)  Although for LBM the groups were comparable at baseline, the summary effect of the intervention still showed no difference between the exercise and standard care groups following an individualised and supervised resistance strengthening exercise programme. Because the two studies assessed the long-term effects of the strengthening exercise programme on LBM and found persistent significant increases in LBM after cessation of the intervention, it could be that the treatment effect only becomes apparent in the long run and that longer follow-up periods need to be explored in future research. Furthermore, Ebid et al. (2012) conducted a trial among adults and reported a significant improvement in muscle strength and LBM for long-term burn patients and comparable non-injured adults following the same isokinetic training programme. This supports the potential benefit for long-term patients and implies that burn patients respond in the same way as non-injured controls (Ebid et al. 2012).
Small sample sizes and poor methodological quality (low PEDro scores) could also contribute to the inconclusive evidence that resistance strengthening exercises post-burn is effective in improving muscle strength and LBM. Blinding of subjects and therapists is challenging, as participation in the 12-week exercise programme compared to the standard care group would be evident. However, blinding of the assessors, concealed allocation and reporting measures of variability are possible, thus limiting the measurement bias.  Including both children and adolescents in one group could also have influenced the results. A review by Schranz, Tomkinson and Olds (2013) found that age (as defined as younger and older than 12 years) has a significant effect on muscle strength following a resistance exercise strengthening programme, where the older adolescent responded more favourably to the intervention compared to the younger child. Future studies should investigate resistance strength training in children separately from adolescents.

PRE Study or Subgroup Mean SD Total Mean SD Total
Nevertheless, individual studies have reported significant within-group improvement in either or both LBM and muscle strength post-intervention, indicating that a resistance strengthening exercise programme could potentially be beneficial for children and adolescents with burns in improving LBM and muscle strength. Improvement in muscle strength is attributed to increased amounts of newly acquired actin and myosin proteins in the muscular contractile apparatus and an increased amount of contractile protein causes muscle hypertrophy, thus also leading to an increased total LBM. Although it appears that there is some merit in implementing supervised individualised isokinetic strength training for children and adolescents with burns 1 month post-burn injury, only one study by Ebid et al. (2014) implemented this strategy; thus, it remains inconclusive and more similar studies are required. Improved LBM and muscle strength might contribute to better quality of life and functional abilities, enabling children and adolescents to successfully reintegrate into their communities.
Future studies should focus on improving the methodological quality of the studies to confirm the treatment effect of a resistance strengthening exercise programme on muscle strength and LBM. Only one study (Ebid et al. 2012) was not conducted in the United States, and the other six studies were implemented at the same institution. This increases selection bias as only participants within a particular geographical area could potentially participant in these studies. Therefore, future research should be implemented internationally to be able to generalise findings and apply them globally to children and adolescents. Studies should lengthen the time period for data collection post-intervention to obtain an indication of the long-term effects of a resistance strengthening exercise programme on muscle strength and LBM.

Conclusion
This review concludes that, at present, there is no substantial evidence to support the added benefit of a resistance strengthening exercise programme for children and adolescents with burns in terms of muscle strength and LBM. Because no deterioration of participants' muscle strength and LBM was reported post-intervention, it appears that there is some merit in implementing supervised individualised isokinetic strength training for children and adolescents with burns; however, future research should pursue further investigation into the effectiveness of a resistance strengthening exercise programme on muscle strength and LBM.