Clinical exercise testing in pediatric rehabilitation Bolster, E.A.M.
2018
document version
Publisher's PDF, also known as Version of record
Link to publication in VU Research Portal
citation for published version (APA)
Bolster, E. A. M. (2018). Clinical exercise testing in pediatric rehabilitation.
General rights
Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights.
• Users may download and print one copy of any publication from the public portal for the purpose of private study or research.
• You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ?
Take down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.
E-mail address:
vuresearchportal.ub@vu.nl
Energy cost during walking in association with age and body height in children and young adults with cerebral palsy
EAM Bolster, ACJ Balemans, MA Brehm, AI Buizer, AJ Dallmeijer
Gait Posture 2017; 54: 119-26
5
AbstrAct
AIM: This cross-sectional study into children and young adults with cerebral palsy (CP) aimed to assess the association of gross energy cost (EC), net EC and net nondimensional (NN) EC during walking with age and body height, compared to typically developing (TD) peers.
MEtHOD: Data was collected in 128 participants with CP (mean age 11y9mo;
GMFCS I, n = 48; II, n = 56; III, n = 24) and in 63 TD peers (mean age 12y5mo). Energy cost was assessed by measuring the oxygen consumption during over-ground walking at comfortable speed. Outcome measures derived from the assessment included the gross and net EC, and NN EC. Differences between the groups in the association between gross, net and NN EC with age and body height, were investigated with regression analyses and interaction effects (p < 0.05).
rEsULts: Interaction effects for age and body height by group were not significant, indicating similar associations for gross, net and NN EC with age or body height among groups. The models showed a significant decline for gross, net and NN EC with increasing age per year (respectively -0.201 J·kg-1·m-1; -0.073 J·kg-1·m-1; -0.007) and body height per cm (respectively -0.057 J·kg-1·m-1; -0.021 J·kg-1·m-1; -0.002).
INtErPrEtAtION: Despite higher gross and net EC values for CP compared to TD participants, similar declines in EC outcomes can be expected with growth for participants aged 4–22 years with CP. All energy cost outcomes showed a decline with growth, indicating that correcting for this decline is required when evaluating changes in gross EC, and, to a lesser extent, in net and NN EC in response to treatment or from natural course over time.
5
INtrODUctION
Children and young adults with cerebral palsy (CP) often have a pathological gait pattern, which can occur due to muscle weakness, abnormal motor control, spasticity, abnormal muscle length and/or bony deformities. It is well established that associated with this gait pathology, energy cost during walking (EC) in children and young adults with CP is often increased compared to typically developing (TD) peers,1-4 and that EC increases with larger motor involvement (higher gross motor function classification system (GMFCS) level5).1,4,6-8 An elevated EC can lead to activity limitations6 and affect the level of daily physical activity.9
In the literature, the EC is presented both in gross and net values. The gross EC is defined as the total energy used per unit of distance covered, expressed in J·kg-1 per meter (J·kg-1·m-1).
When normalization for resting energy consumption is required, for example to control for the effects of growth and development, the net EC can be calculated by subtracting the resting energy consumption from the gross energy consumption. By doing so, the net EC gives a more direct indication of the walking energy cost because it is independent of resting energy consumption.10 On the other hand, compared to the gross EC, the net EC has a lower reliability, resulting from the additional measurement error of the resting energy consumption measurement.2 To decrease the variability in resting energy consumption and thereby improve the reliability of the net EC, two recommendations are described in the literature 1) abstinence from food intake and exercise for at least four to 12 h prior to testing11,12 and 2) multiple repeated testing.2 However, for clinical purposes this is not always feasible and therefore the gross EC is still used for cross-sectional evaluation, although for longitudinal evaluations the net EC is more suitable.
A normalization procedure for the net EC is the nondimensional scheme, described by Schwartz et al.10 It is assumed that the net nondimensional (NN) EC is an even better variable for longitudinal evaluations, because this outcome is essentially independent of body height, weight and mass and therefore the NN EC is the preferred method compared to the gross EC.10 However, a disadvantage of the NN EC is that this outcome is more difficult to interpret for clinicians. Therefore, the gross and net EC are often used in clinical settings. For the evaluation of changes in EC after interventions, such as orthotics or surgical interventions, it is important to know the normal development of the different EC outcomes (gross, net and NN) over time in children and young adults with CP.
For TD children, the gross EC declined with aging, while the net EC showed a more gradual decline with increasing age until adulthood.13 Data of 168 TD children between the ages
of 2.8 and 18.6 years showed that the NN EC is essentially independent of body height, weight and mass.10 For children with CP, different trends for the association between EC and age have been presented. Gross EC showed a significant but small decline with age for children between the age of 4 and 18.8 For the net EC, Marconi et al. found a decline of net EC with increasing age for younger CP children and a stabilization from 12 to 14 years.14 Kerr et al. described that the association between net oxygen cost and age was best presented by a quadratic model with the turning point of the curve occurring at the age of 12 years meaning that gait is least economic at this age, and stays equal or improves beyond this age.15 For the NN EC, children classified as GMFCS levels I, II and III all had an increase in the NN EC over one year.4 This was the first longitudinal study and these results have not been confirmed by other studies. Taken together, how the EC develops with growth for the different GMFCS levels compared to TD peers is not completely understood, also because most studies only focused on the development of gross EC or NN EC. To our knowledge there is no study that compared all three EC outcomes (gross, net and NN EC) in children and young adults with CP. Thereby, differences between the development for children and young adults with CP compared to TD peers have not yet been described, while this information is necessary to select the most appropriate outcome for research and clinical purposes.
This cross-sectional study into children and young adults with CP (GMFCS levels I–III) aimed to assess the association of gross EC, net EC and NN EC with age and body height, and compare this with TD peers.
MEtHODs
Participants
EC data from different research projects3,16,17 and from our clinical exercise laboratory outpatient clinic of the Department of Rehabilitation Medicine at the VU University Medical Center in Amsterdam, measured between 2006 and 2014 were used. TD participants were recruited through departmental colleagues and via different schools in and around Amsterdam. Data of participants between 4 and 22 years of age were included and the participants with CP had to be classified as GMFCS levels I, II or III. Participants were excluded when they had an orthopaedic or neuro-surgical treatment in the past 12 months or botulinum toxin treatment in the past three months. Participants were also excluded when walking speed was less than 24 m per minute (or 0.4 m per second), as these participants appeared not to be functional walkers in daily life. The institutional
5
ethics committee of the VU University Medical Center approved for the retrospective data included in this study collected from different studies,16,17 and for the use of the clinical data they decided that the study did not fall under the scope of the Medical Research Involving Human Subjects Act (WMO).
Procedure
Each EC test consisted of a rest test followed by a walk test. First, body height (cm) and weight (kg) were determined standing on an electronic scale. Second, energy consumption during resting and walking was measured using a lightweight, portable gas-analysis system (Metamax 3B Cortex Biophysik, Leipzig, Germany). Before each participant was tested, this system was calibrated according to the manufacturers recommendations.
Fitting of the facemask was carefully inspected for leakage. The participants were given specific instructions not to eat or drink (except for water) 1.5 h before testing. Oxygen uptake (VO2) and carbon dioxide production (VCO2) values were measured breath by breath during a five min resting period (lying or sitting on a bench while watching a video) and during six minutes of walking at a comfortable, self-chosen speed on an indoor oval track (40 m), while they used their typical walking aids and/or orthotics.
The distance covered during the walking test was registered in order to calculate the walking speed (m·min-1 and m·s-1). Heart rate (b·min-1) was registered with a flexible heart rate monitor (Polar FT7, Kempele, Finland).
Outcome measures
The mean walking speed (m·min-1 and m·s-1) was calculated as the distance walked in 6 min divided by 6. Breath by breath respiratory-exchange ratios (RERs) were calculated as VCO2 divided by VO2. The steady state was visually inspected and defined as two minutes of the whole test (excluding the first two minutes) in which fluctuations in walking speed, VO2 and VCO2 showed the least change and RER was below 1.0.10 The mean oxygen uptake values (VO2, in ml·kg-1·min-1) and RERs were computed over these steady state periods and used to calculate the average steady state resting and gross energy consumption (ECSrest and ECSgross, both in J·kg-1·min-1), calculated by (4.960 x RER + 16.040) x VO2 (ml·kg-1·min-1).18 The net energy consumption (ECSnet) was calculated by ECSgross - ECSrest. Gross EC and net EC were than calculated by dividing the ECSgross and ECSnet by walking speed (m·min-1), expressed in J·kg-1·m-1. The NN EC was calculated according to the nondimensional normalization scheme described by Schwartz et al. (Appendix 5.1).10 The mean heart rate (b·min-1) was calculated over the same steady state period.
statistical analyses
Distribution of the data was checked using inspection of mean values, standard deviations, and using visual inspection of the histograms and normal Q–Q plots. As the data were normally distributed, parametric tests were applied. Participants’ characteristics of the different groups were compared using a one-way ANOVA with Bonferroni adjustments.
An ANOVA was also used to test for differences between the GMFCS levels and TD participants for the different walking parameters, including gross, net and NN EC. The gross and net EC were adjusted for age and body height and the NN EC only for age.
To assess the differences in the associations of gross EC, net and NN EC with age and body height between GMFCS levels I, II, III and TD participants, linear regression analyses were performed with interaction effects specified for age and body height by group. Gross, net and NN EC were the dependent variables and age, body height and diagnosis (GMFCS levels I, II, III and TD) the independent variables. Except for diagnosis (categorical data), both the dependent and independent variables were continues data. A significance level of p < 0.05 was used for all statistical tests. The analyses were performed using Statistical Package for the Social Science, version 22.0 (SPSS Inc, Chicago, IL, USA).
rEsULts
Characteristics of children and young adults with CP (n = 128) for GMFCS levels I, II and III and TD peers (n = 63) are shown in Table 5.1. Characteristics between groups were comparable, except for body height (p = 0.045). For 11 participants with CP, the resting energy consumption was not measured correctly, because these participants were not able to lie or sit (still) on a bench for 5 min. Therefore, the net EC and NN EC were calculated for 180 participants. Overall, the gross EC, net EC and NN EC, adjusted for age and body height, were significantly different between CP and TD participants, and between GMFCS levels (Table 5.2). All energy cost outcomes showed higher values for CP participants in comparison with TD peers, and higher values for higher GMFCS levels. For example, the gross EC values for GMFCS level I (5.90 J·kg-1·m-1), II (7.69 J·kg-1·m-1) and III (10.89 J·kg-1·m-1) were higher than for TD participants (4.93 J·kg-1·m-1).
In Figure 5.1, the associations for gross EC, net EC and NN EC with age and body height are shown for the different groups. Regression analyses showed that there were no interaction effects for age and body height by group for gross EC, net EC and NN EC (for complete models see Appendices 5.2 and 5.3). This indicates similar associations (i.e.
declines) of gross EC, net EC and NN EC with age and body height among groups. The
5
table 5.1 characteristics of the 191 participants divided in children and young adults with cP in GMFcs levels I, II and III, and tD peers TD (n = 63)GMFCS I (n = 48)GMFCS II (n = 56)GMFCS III (n = 24)FpPost hoc Boys / girls [n]27 / 3629 / 1934 / 2214 / 10-0.533- Age [y mo] mean (SD; range)12y5mo (4y11mo; 6y – 22y) 10y8mo (3y9mo; 4y – 22y)12y8mo (4y3mo; 4y – 22y)11y6mo (4y3mo; 5y – 22y)2.0770.105- Body height [cm] mean (SD; range)151.6 (18.3; 122 – 200)142.9 (19.0; 95 – 185)149.3 (18.3; 112 – 183)142.3 (20.1; 100 – 180)2.7270.045- Weight [kg] mean (SD; range)44.1 (18.7; 20 – 118)37.8 (14.6; 17 – 75)43.6 (14.7; 19 – 73)39.5 (16.8; 13 – 79)1.7180.165- TD, typically developing; GMFCS, gross motor function classification system.
Figure 5.1
A Association between gross energy cost and age*.
B Association between gross energy cost and body height*.
C Association between net energy cost and age*.
D Association between net energy cost and body height*.
E Association between net nondimensional energy cost and age*.
F Association between net nondimensional energy cost and body height*.
* For the different GMFCS levels in CP and TD. Black = TD; Green = GMFCS I; Blue = GMFCS II; Red = GMFCS III (regression lines are shown for each group separately).
A
C
E F
D B
5
table 5.2 Mean (sE) of different energy cost outcomes, adjusted for age and body height, in chil- dren and young adults with cP per GMFcs level and tD peers (n = 191)
TD
(n = 63) GMFCS I
(n = 48) GMFCS II
(n = 56) GMFCS III
(n = 24) F p Post hoc
Gross EC
[J·kg-1·m-1] 4.93
(0.19) 5.90
(0.22) 7.69
(0.20) 10.89
(0.31) 101.459 < 0.001 TD–I, TD–II, TD–III, I–II, I–III, II–III Net EC *
[J·kg-1·m-1] 3.11
(0.16) 4.00 (0.20) [n = 42]
5.45 (0.17) [n = 53]
7.68 (0.27) [n = 22]
79.750 < 0.001 TD–I, TD–II, TD–III, I–II, I–III, II–III NN EC* / ** 0.31
(0.02) 0.41 (0.02) [n = 42]
0.56 (0.02) [n = 53]
0.79 (0.03) [n = 22]
84.839 < 0.001 TD–I, TD–II, TD–III, I–II, I–III, II–III VO2walk
[ml·kg-1·min-1] 18.46
(0.58) 20.81
(0.67) 22.75
(0.62) 25.09
(0.95) 14.891 < 0.001 TD–II, TD–III, I–III Walking RER 0.78
(0.01) 0.83
(0.01) 0.86
(0.01) 0.85
(0.02) 8.773 < 0.001 TD–I, TD–II, TD–III Walking speed
[m·min-1] 75.5
(1.2) 71.8
(1.4) 60.8
(1.3) 49.6
(1.9) 58.367 < 0.001 TD–II, TD–III, I–II, I–III, II–III Walking speed
[m·s-1] 1.26
(0.02) 1.20
(0.02) 1.01
(0.02) 0.81
(0.03) 58.367 < 0.001 TD–II, TD–III, I–II, I–III, II–III Walking heart
rate [b·min-1] 109.9 (2.2) 123.3
(3.3) 137.1
(2.5) 144.5
(4.5) 29.030 < 0.001 TD–I, TD–II, TD–III, I–II, I–III
TD, typically developing; GMFCS, gross motor function classification system; EC, energy cost; NN, net nondimensional; VO2walk, oxygen uptake during walking; RER, respiratory exchange ratio; –, significantly different between the two groups (p < 0.05).
* n = 180.
** Adjusted for age.
analyses for the total group showed a significant decline for the gross EC of 0.201 J·kg-1·m-1 per year (SE 0.027 J·kg-1·m-1; p < 0.001) with increasing age or a decline of 0.057 J·kg-1·m-1 per centimeter (SE 0.006 J·kg-1·m-1; p < 0.001) with increasing body height. The net and NN EC showed a similar, though relatively smaller decline with increasing age and body height (Tables 5.3 and 5.4).
table 5.3Association of gross, net and NN Ec during walking with age in children and young adults with GMFcs levels I, II and III in comparison with tD peers Gross EC [J·kg-1·m-1] (n = 191)*Net EC [J·kg-1·m-1] (n = 180)**NN EC (n = 180)*** Model B (SE)95% CIpB (SE)B (95% CI)pB (SE)B (95% CI)p Constant Group TD (reference) GMFCS I GMFCS II GMFCS III Age 7.186 (0.391) 0 1.115 (0.312) 2.950 (0.296) 6.345 (0.387) -0.201 (0.027) 6.414 – 7.957 0.500 – 1.730 2.367 – 3.534 5.582 – 7.108 -0.254 – -0.148
< 0.001 < 0.001 < 0.001 < 0.001 < 0.001
3.968 (0.323) 0 0.923 (0.258) 2.403 (0.240) 4.679 (0.319) -0.073 (0.023) 3.330 – 4.605 0.415 – 1.432 1.929 – 2.876 4.050 – 5.308 -0.118 – -0.029
< 0.001 < 0.001 < 0.001 < 0.001 0.001
0.405 (0.033) 0 0.094 (0.026) 0.245 (0.024) 0.478 (0.033) -0.007 (0.002) 0.340 – 0.470 0.042 – 0.145 0.197 – 0.294 0.414 – 0.542 -0.012 – -0.003
< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 EC, energy cost; NN, net nondimensional; TD, typically developing; GMFCS, gross motor function classification system; * R2 for model with group only = 0.56 (p < 0.001), R2 for model with group and age = 0.66 (p < 0.001); ** R2 for model with group only = 0.58 (p < 0.001), R2 for model with group and age = 0.61 (p < 0.001); *** R2 for model with group only = 0.58 (p < 0.001), R2 for model with group and age = 0.60 (p < 0.001).
5
table 5.4Association of gross, net and NN energy cost during walking with body height in children and young adults with different GMFcs levels in comparison with tD peers Gross EC [J·kg-1·m-1] (n = 191)*Net EC [J·kg-1·m-1] (n = 180)**NN EC (n = 180)*** Model B (SE)95% CIpB (SE)B (95% CI)pB (SE)B (95% CI)p Constant Group TD (reference) GMFCS I GMFCS II GMFCS III Body height 13.311 (0.903) 0 0.969 (0.290) 2.780 (0.274) 5.990 (0.362) -0.057 (0.006) 11.586 – 15.106 0.397 – 1.542 2.239 – 3.321 5.276 – 6.704 -0.068 – -0.046
< 0.001 0.001 < 0.001 < 0.001 < 0.001
6.307 (0.833) 0 0.891 (0.255) 2.334 (0.237) 4.572 (0.316) -0.021 (0.005) 4.664 – 7.950 0.389 – 1.394 1.866 – 2.801 3.949 – 5.196 -0.032 – -0.011
< 0.001 0.001 < 0.001 < 0.001 < 0.001
0.644 (0.085) 0 0.091 (0.026) 0.238 (0.024) 0.467 (0.032) -0.002 (0.001) 0.476 – 0.812 0.040 – 0.142 0.191 – 0.286 0.403 – 0.530 -0.003 – -0.001
< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 EC, energy cost; NN, net nondimensional; TD, typically developing; GMFCS, gross motor function classification system; * R2 for model with group only = 0.56 (p < 0.001), R2 for model with group and body height = 0.71 (p < 0.001); ** R2 for model with group only = 0.58 (p < 0.001), R2 for model with group and body height = 0.61 (p < 0.001); *** R2 for model with group only = 0.58 (p < 0.001), R2 for model with group and body height = 0.62 (p < 0.001).
DIscUssION
This cross-sectional study into children and young adults with CP (GMFCS levels I–III) aimed to assess the association of gross EC, net EC and NN EC with age and body height in comparison with TD peers. Our results showed that, despite much higher energy cost outcomes for participants with CP, the decline of gross EC, net EC and NN EC with age and body height were similar for children and young adults with CP classified as GMFCS levels I, II, III and TD peers. In addition, we found that the gross EC, net EC and NN EC significantly declined with growth for CP and TD participants. This decline was larger for gross EC than for net EC and NN EC. So, for long-term follow-up assessments, for example when evaluating changes following treatment after one year, it should be taken into account that all three outcomes (gross, net and NN EC) decline with growth both for CP and TD participants (Table 5.4).
This is the first study that assessed the decline in EC for three different outcomes in participants with CP, showing that the decline in gross EC per year was higher (-0.201 J·kg-1·m-1 (representing -3% of the mean)) compared to the decline in net EC (-0.073 J·kg-1·m-1 (-1.6%)) and NN EC (-0.007 (-1.5%)). These results are in agreement with other studies where net values were also less sensitive to growth than the gross EC.10,13 So, for long-term follow-up assessments we advise the use of net values when evaluating changes over time.
The decline in net and NN EC with growth in our study were comparable, indicating that both outcomes are less sensitive to growth compared to the gross outcome. Although it is suggested that the NN EC is the preferred method for reporting oxygen or energy consumption data for children during growth,7,10 our study indicated that using the net EC reveals similar results. In the nondimensional normalization scheme, walking speed and energy consumption are corrected for leg length. However, the NN EC is not corrected for leg length (Appendix 5.1).10 Van der Walle et al.13 also reported on the net EC and NN EC, though in a group of TD participants between the age of 3 and 33 years, and, likewise, found that the decline in both outcomes was similar. Based on these results and considering the fact that a disadvantage of the NN EC is that this outcome is harder to interpret for clinicians than the net EC, we propose, that the net EC is as good as the NN EC for longitudinal evaluations in children. However, for comparing walking speed and energy consumption (J·kg-1·min-1) over time, using the nondimensional normalization scheme seems preferable.
When comparing the gross EC, net EC and NN EC with reference values, it should be taken into account that these outcomes decline both with age and body height, as our
5
study shows. Determining reference values should therefore be based on age and/or body height. In order to determine which outcome variable is the most appropriate to use, we compared the explained variance for age and body height of the regression models in addition to the GMFCS level. The explained variance of age, ranging from +2% to +10%, was somewhat smaller in comparison with body height, ranging from +3% to 15%. A possible explanation for this is the difference in body height between participants with CP and TD; TD children and young adults are generally taller than participants with CP of the same age.19 Reference values based on body height may therefore seem more appropriate than references values based on age when comparing CP children and young adults with TD peers. However, this difference was only small and in clinical settings the assessment of body height for participants with CP is not always reliable because of bony deformities and abnormal muscle length. Therefore, we recommend that age-based reference values of TD participants should preferably be used.
Several studies confirm that TD children and young adults become more economic in walking when they get older.13,20,21 Our data shows that similar results can be expected for participants with CP. The decline we found with increasing age (-0.201 J·kg-1·m-1) was slightly larger than the decline Kamp et al.8 found in their study for the gross EC (-0.16 J·kg-1·m-1). They only included participants with CP classified as GMFCS levels I, II and III between the age of 4 and 18, while we included participants between the age of 4 and 22.8 as well as TD participants. The inclusion of TD participants in our study could explain the difference in the amount of decline. Participants with CP experience motor impairments when they grow due to an increase in bony deformities, abnormal muscle length and muscle weakness, while TD peers experience no motor impairments when they grow. We assume that due to the increase in motor impairments, the gross EC might show less decline over time in comparison with TD peers. Nevertheless, our results suggest that the development of the gross EC over time is similar for children and young adults with CP and TD peers.
The net and NN EC showed a similar decline with age and body height for participants with CP and TD between the age of 4 and 22. The quadratic model described in the study of Kerr et al.6 (age range 4–16 years) could not be replicated for the net values in our study or other studies. The stabilization of the net EC from the age of 12–14 years found in the study of Marconi et al.14 could also not be confirmed with our results. Although we found a linear relation in participants aged 4–22 years, it has to be noted that this relation is probably not linear when younger and older individuals are included. Thomas et al.4 found that children with CP (age 5.6–18 years; GMFCS level I–III) showed an increase in NN EC over one year, where we found a decline. A weakness of our study is the use of
cross-sectional data, where Thomas et al.4 used longitudinal data. Yet, in the Thomas study, only 34 children with CP were included, while our study sample included 128 participants with CP. Among these 128 participants we found that the within group variation for the NN EC (and also for the gross and net EC) increased by an increase in GMFCS level, showing larger variation for GMFCS levels II and III. Both for the net EC and NN EC there seems to be a trend for a stabilization of the net EC and NN EC with growth for GMFCS levels II and III. The large variation within these groups could be an explanation for the fact that the interaction effects for groups were not significant in this study and that we did not find a stabilization of the net EC or an increase in the NN EC, contrary to Marconi et al.14 and Thomas et al.4 Further studies could focus on the longitudinal development of energy cost for confidently accepting the results we found.
Besides the development over time, it would be useful to assess the differences over time between the different GMFCS levels with longitudinal data.
study limitations
A limitation of this study is that we used cross-sectional data in order to assess the association of gross EC, net EC and NN EC with age and body height over time.
cONcLUsION
Despite higher gross EC, net EC and NN EC values for children and young adults with CP, this cross-sectional study shows that similar declines in energy cost outcomes can be expected with growth for children and young adults with CP compared to TD peers.
The gross EC, net EC and NN EC decline when CP and TD children and young adults get older or taller, and this decline was somewhat larger for gross EC than for net EC and NN EC. These results indicate that correcting for this decline over time is needed when evaluating changes in EC in response to treatment or from natural course. Further longitudinal studies should confirm these results.
AcKNOWLEDGEMENts
This study was supported by a grant from Foundation Nuts Ohra (1301-059) and Phelps Foundation for Spastics (2013-008). They were not involved in the design of the study, data collection, data analysis, manuscript preparation, and publication decisions. All children, adolescents and parents are acknowledged for their willingness to participate in this study.
5
rEFErENcEs
1 Johnston TE, Moore SE, Quinn LT, Smith BT. Energy cost of walking in children with cerebral palsy: relation to the Gross Motor Function Classification System. Dev Med Child Neurol 2004; 46: 34-8.
2 Brehm MA, Becher J, Harlaar J. Reproducibility evaluation of gross and net walking efficiency in children with cerebral palsy. Dev Med Child Neurol 2007; 49: 45-8.
3 Dallmeijer AJ, Brehm MA. Physical strain of comfortable walking in children with mild cerebral palsy. Disabil Rehabil 2011; 33: 1351-7.
4 Thomas SS, Buckon CE, Russman BS, Sussman MD, Aiona MD. A comparison of the changes in the energy cost of walking between children with cerebral palsy and able- bodied peers over one year. J Pediatr Rehabil Med 2011; 4: 225-33.
5 Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy.
Dev Med Child Neurol 1997; 39: 214-23.
6 Kerr C, Parkes J, Stevenson M, Cosgrove AP, McDowell BC. Energy efficiency in gait, activity, participation, and health status in children with cerebral palsy. Dev Med Child Neurol 2008; 50: 204-10.
7 Thomas SS, Buckon CE, Schwartz MH, Russman BS, Sussman MD, Aiona MD. Variability and minimum detectable change for walking energy efficiency variables in children with cerebral palsy. Dev Med Child Neurol 2009; 51: 615-21.
8 Kamp FA, Lennon N, Holmes L, Dallmeijer AJ, Henley J, Miller F. Energy cost of walking in children with spastic cerebral palsy: relationship with age, body composition and mobility capacity. Gait Posture 2014; 40: 209-14.
9 Maltais DB, Pierrynowski MR, Galea VA, Bar-Or O. Physical activity level is associated with the O2 cost of walking in cerebral palsy. Med Sci Sports Exerc 2005; 37: 347-53.
10 Schwartz MH, Koop SE, Bourke JL, Baker R. A nondimensional normalization scheme for oxygen utilization data. Gait Posture 2006; 24: 14-22.
11 Schwartz MH. Protocol changes can improve the reliability of net oxygen cost data.
Gait Posture 2007; 26: 494-500.
12 Haugen HA, Melanson EL, Tran ZV, Kearney JT, Hill JO. Variability of measured resting metabolic rate. Am J Clin Nutr 2003; 78: 1141-5.
13 Van de Walle P, Desloovere K, Truijen S, Gosselink R, Aerts P, Hallemans A. Age-related changes in mechanical and metabolic energy during typical gait. Gait Posture 2010; 31:
495-501.
14 Marconi V, Carraro E, Trevisi E, Capelli C, Martinuzzi A, Zamparo P. The Locomotory Index in diplegic and hemiplegic children: the effects of age and speed on the energy cost of walking. Eur J Phys Rehabil Med 2012; 48: 403-12.
15 Kerr C, McDowell BC, Parkes J, Stevenson M, Cosgrove AP. Age-related changes in energy efficiency of gait, activity, and participation in children with cerebral palsy. Dev Med Child Neurol 2011; 53: 61-7.
16 Scholtes VA, Dallmeijer AJ, Knol DL, Speth LA, Maathuis CG, Jongerius PH, Becher JG.
The combined effect of lower-limb multilevel botulinum toxin type a and comprehensive rehabilitation on mobility in children with cerebral palsy: a randomized clinical trial.
Arch Phys Med Rehabil 2006; 87: 1551-8.
17 Brehm MA, Scholtes VA, Dallmeijer AJ, Twisk JW, Harlaar J. The importance of addressing heteroscedasticity in the reliability analysis of ratio-scaled variables: an example based on walking energy-cost measurements. Dev Med Child Neurol 2012; 54:
267-73.
18 Garby L, Astrup A. The relationship between the respiratory quotient and the energy equivalent of oxygen during simultaneous glucose and lipid oxidation and lipogenesis.
Acta Physiol Scand 1987; 129: 443-4.
19 Krick J, Murphy-Miller P, Zeger S, Wright E. Pattern of growth in children with cerebral palsy. J Am Diet Assoc 1996; 96: 680-5.
20 Waters RL, Mulroy S. The energy expenditure of normal and pathologic gait. Gait Posture 1999; 9: 207-31.
21 DeJaeger D, Willems PA, Heglund NC. The energy cost of walking in children. Pflugers Arch 2001; 441: 538-43.
5
Appendix 5.1 Formulas used for the calculation of the gross, net and net nondimensional (NN) energy cost (Ec)
Gross energy cost
Gross EC (J·kg-1·m-1) = ECSgross / v
ECSgross = energy consumption during walking (J·kg-1·s-1) v = walking speed (m·s-1)
Net energy cost
Net EC (J·kg-1·m-1) = (ECSgross - ECSrest) / v
ECSgross = energy consumption during walking (J·kg-1·s-1) ECSrest = energy consumption during resting (J·kg-1·s-1) v = walking speed (m·s-1)
Nondimensional energy cost
NN EC = ((ECSgross - ECSrest) / v) · (1 / (m·g))
ECSgross = energy consumption during walking (J·s-1) ECSrest = energy consumption during resting (J·s-1) v = walking speed (m·s-1)
m = body weight (kg) g = gravity = 9.81 (m·s2)
Appendix 5.2Interaction effects of gross Ec, net Ec and NN Ec with age in children and young adults with different GMFcs levels in comparison with tD peers Gross EC [J·kg-1·m-1] in relation to age (n = 191)Net EC [J·kg-1·m-1] in relation to age (n = 180)NN EC in relation to age (n = 180) Model B (SE)95% CIpB (SE)95% CIpB (SE)95% CIp Constant Group TD (reference) GMFCS I GMFCS II GMFCS III Age Group x age TD (reference) x age GMFCS I x age GMFCS II x age GMFCS III x age
6.604 (0.551) 0 2.186 (0.909) 3.883 (0.877) 7.356 (1.120) -0.154 (0.041) 0 -0.093 (0.076) -0.075 (0.066) -0.084 (0.090)
5.517 – 7.690 0.392 – 3.979 2.152 – 5.614 5.146 – 9.565 -0.235 – -0.072 -0.243 – 0.058 -0.205 – 0.055 -0.261 – 0.093
< 0.001 0.017 < 0.001 < 0.001 < 0.001 0.226 0.258 0.349
4.266 (0.441) 0 0.885 (0.825) 1.675 (0.722) 3.794 (0.988) -0.097 (0.033) 0 0.001 (0.068) 0.058 (0.054) 0.073 (0.077)
3.396 – 5.136 -0.743 – 2.512 0.251 – 3.100 1.844 – 5.745 -0.163 – -0.032 -0.134 – 0.136 -0.049 – 0.164 -0.080 – 0.255
<0.001 0.285 0.021 <0.001 0.004 0.990 0.286 0.347
0.436 (0.045) 0 0.090 (0.084) 0.171 (0.074) 0.387 (0.101) -0.010 (0.003) 0 0.000 (0.007) 0.006 (0.005) 0.007 (0.008)
0.347 – 0.524 -0.076 – 0.256 0.026 – 0.316 0.188 – 0.587 -0.017 – -0.003 -0.014 – 0.014 -0.005 – 0.017 -0.008 – 0.023
0.000 0.285 0.021 0.000 0.004 0.990 0.286 0.347 EC, energy cost; NN, net nondimensional; TD, typically developing; GMFCS, gross motor function classification system.
5
Appendix 5.3Interaction effects of gross Ec, net Ec and NN Ec with body height in children and young adults with different GMFcs levels in comparison with tD peers Gross EC [J·kg-1·m-1] in relation to body height (n = 191)Net EC [J·kg-1·m-1] in relation to body height (n = 180)NN EC in relation to body height (n = 180) Model B (SE)(95% CI)pB (SE)95% CIpB (SE)95% CIp Constant Group TD (reference) GMFCS I GMFCS II GMFCS III Body height Group x body height TD (reference) x body height GMFCS I x body height GMFCS II x body height GMFCS III x body height
11.477 (1.580) 0 2.624 (2.285) 5.087 (2.280) 11.077 (2.723) -0.045 (0.010) 0 -0.011 (0.015) -0.015 (0.015) -0.035 (0.019)
8.359 – 14.594 -1.884 – 7.133 0.588 – 9.586 5.704 – 16.449 -0.065 – -0.024 -0.041 – 0.020 -0.045 – 0.014 -0.72 – 0.002
< 0.001 0.252 0.027 < 0.001 < 0.001 0.483 0.312 0.062
6.962 (1.356) 0 0.298 (2.211) 1.146 (2.023 3.136 (2.663) -0.026 (0.009) 0 0.004 (0.015) 0.008 (0.013) 0.010 (0.018)
4.286 – 9.639 -4.066 – 4.662 -2.846 – 5.138 -2.121 – 8.392 -0.043 – -0.008 -0.025 – 0.033 -0.018 – 0.034 -0.026 – 0.045
< 0.001 0.893 0.572 0.241 0.004 0.793 0.556 0.591
0.711 (0.138) 0 0.030 (0.226) 0.117 (0.206) 0.320 (0.272) -0.003 (0.001) 0 0.000 (0.002) 0.001 (0.001) 0.001 (0.002)
0.438 – 0.984 -0.415 – 0.476 -0.291 – 0.525 -0.217 – 0.857 -0.004 – -0.001 -0.003 – 0.003 -0.002 – 0.003 -0.003 – 0.005
< 0.001 0.893 0.572 0.241 0.004 0.793 0.556 0.591 EC, energy cost; NN, net nondimensional; TD, typically developing; GMFCS, gross motor function classification system.
