Abstract
Background Dynamometry has been used extensively to measure knee extensor strength in individuals with cerebral palsy (CP). However, increased coactivation can lead to underestimation of knee extensor strength and, therefore, reduce validity of strength measurements. It is yet unknown to what extent coactivation occurs during dynamometry testing and whether coactivation is influenced by severity of CP, load levels, and muscle fatigue.
Objectives The aims of this study were: (1) to investigate coactivation in adolescents with and without CP during dynamometer tests and (2) to assess the effect of Gross Motor Function Classification System (GMFCS) level, load level, and muscle fatigue on coactivation.
Design A cross-sectional observational design was used.
Method Sixteen adolescents with CP (GMFCS levels I and II: n=10/6; age range=13–19 years) and 15 adolescents without CP (n=15; age range=12–19 years) performed maximal isometric contractions (maximal voluntary torque [MVT]) and a series of submaximal dynamic contractions at low (±65% MVT), medium (±75% MVT), and high (±85% MVT) loads until fatigue. A coactivation index (CAI) was calculated for each contraction from surface electromyography recordings from the quadriceps and hamstring muscles.
Results Adolescents with CP classified in GMFCS level II showed significantly higher CAI values than adolescents classified in GMFCS level I and those without CP during maximal and submaximal contractions. No differences were observed among load levels. During the series of fatiguing submaximal contractions, CAI remained constant in both the CP group and the group with typical development (TD), except for adolescents with TD at the low-load condition, which showed a significant decrease.
Limitations Electromyography tracings were normalized to amplitudes during maximal isometric contractions, whereas previous studies suggested that these types of contractions could not be reliably determined in the CP population.
Conclusion Coactivation was higher in adolescents with CP classified in GMFCS level II than in adolescents with TD and those with CP in GMFCS level I at different load levels. Within all groups, coactivation was independent of load level and fatigue. In individuals with CP, coactivation can lead to an underestimation of agonist muscle strength, which should be taken into account while interpreting the results of both maximal and submaximal dynamometer tests.
Cerebral palsy (CP) is the most common movement disorder in children, with an incidence of 2 per 1,000 live births.1 The primary motor deficits observed in individuals with CP are muscle paresis, muscle spasticity, and impaired selective motor control.2 These motor deficits can provoke muscle weakness in individuals with CP, especially in the lower limb muscles.3 Because there are indications that lower limb muscle strength is related to mobility limitations in individuals with CP,4,5 there has been increasing interest in studying the effectiveness of muscle strength training programs.6–9 In order to determine proper training intensities in such programs and to evaluate their effectiveness, valid and reliable assessments of muscle strength are needed.
To investigate muscle strength in the CP population, different methods are used in clinical practice and research. Muscle strength is widely expressed as maximal voluntary isometric strength, assessed using computer-controlled or handheld dynamometers.3,10–12 It has been shown, however, that many individuals with CP have difficulty in maximally recruiting their muscles,13 which reduces the validity of maximal strength measurements. Therefore, in more recent research, submaximal strength tests were used, with strength expressed in terms of the repetition maximum (RM) at submaximal load.14–18 During these different types of dynamometer measurements, a net moment around the joint is measured. This net moment is the resultant moment generated by the agonists and the antagonists, requiring the agonistic muscle group to be selectively activated to validly assess agonistic muscle strength. In people who are able-bodied, a well-balanced interaction between excitation of the agonist and a proportional inhibition of its antagonist is facilitated through the mechanism of reciprocal inhibition.19 Some studies, however, showed deficits in this reciprocal inhibition in children with CP.20,21 High levels of coactivation have been observed in individuals with CP during maximal isometric strength measurements22,23 and during gait.22,24,25 Coactivation can be a motor control strategy, and it is primarily present when an individual needs increased joint stability or improved movement accuracy (eg, while learning a new task).26 However, in line with its inherent inefficiency, excessive coactivation also can impair motor performance. Specifically, for strength testing, higher levels of coactivation can lead to lower net moments.27 As a consequence, an underestimation of the strength of the agonists might occur.2 Therefore, it is important to investigate the level of coactivation in muscle strength tests that are used extensively in clinical practice and research.
Different dynamometer tests are used in clinical practice. Maximal isometric tests have been considered the standard test for strength assessment, but recently submaximal tests have gained popularity. It is known from the literature that an increase of loading on the knee joint leads to an increase of hamstring muscle coactivation for joint stabilization in individuals with typical development (TD).28 However, Grabiner et al29 did not observe any difference in hamstring muscle coactivation with increasing isometric knee extensor force. The present study, therefore, assessed coactivation for different load levels in adolescents with CP and those with TD.
Another factor that potentially affects coactivation level is fatigue. Previous research showed that isokinetic fatiguing contractions did not affect the level of coactivation in children with TD.30,31 In a recent study by Moreau et al32 in children with CP, muscle activation levels of both agonist and antagonist muscles were studied during a series of fatiguing maximal isokinetic knee extension contractions. They observed that, in contrast to children with TD, the CP group showed a high activation of the antagonist muscles, which decreased over the course of the test. The authors suggested that this change in antagonist muscle activation could be a mechanism to preserve knee torque output in the face of fatigue.32 It is unclear, however, whether such a response will occur during submaximal fatiguing contractions. Therefore, we also assessed the effect of fatigue on coactivation in children with CP.
As CP is a heterogenic condition, it is important to acknowledge potential differences in coactivation among individuals with CP. Previous research showed clear differences in maximal muscle strength of individuals with CP classified in different levels of the Gross Motor Function Classification System (GMFCS).33,34 Different levels of coactivation might contribute to these observed differences in muscle strength. To our knowledge, however, no previous studies investigated potential differences in coactivation among people with CP and different GMFCS levels. To adequately interpret the results of muscle strength tests of individuals with CP in clinical practice or research, insight into the potential occurrence of coactivation in individuals with different GMFCS levels is needed.
The aim of this study was to investigate the level of muscle coactivation in adolescents with CP during dynamometer strength measurements and determine the effects of GMFCS level, load level, and fatigue on muscle coactivation. Because muscle coactivation also is present in the population with TD, the results were compared with those of peers with TD.
Method
Participants
This cross-sectional observational study included 16 adolescents with CP (age range=13–19 years) who were recruited in 1 of 2 rehabilitation settings. Adolescents with CP had to have the ability to walk with or without limitations (ie, classified in GMFCS level I or II).33 They were excluded if they had received botulinum toxin treatment within 6 months prior to testing or orthopedic surgery within 12 months prior to testing or if they had unstable seizures, severe orthopedic or cardiopulmonary problems, or other contraindications for maximal exercise. Fourteen age- and sex-matched adolescents with TD (age range=12–19 years) and without a known history of neurological, orthopedic, or cardiovascular diseases also were recruited. The adolescents and parents or legal guardians of adolescents under the age of 18 years signed an informed consent form indicating voluntary participation in the study.
Experimental Setup
Coactivation data were obtained from EMG measurements during maximal isometric tests and a series of submaximal contractions performed on 1 of 2 types of computer-controlled dynamometers (Humac Norm, Lode BV, Groningen, the Netherlands, or Biodex, Biodex Medical Systems Inc, Shirley, New York), depending on location of inclusion. A pilot study demonstrated similar outcomes for these 2 dynamometers with the standardized protocols used.18 Adolescents with CP performed the tests with their most affected leg, as noted in their medical status. Adolescents with TD performed the tests with their preferred leg, with the results assessed using a questionnaire.35 Participants were seated on the chair of the dynamometer and firmly strapped to the seat with the hip flexed at 80 degrees (full extension=0°). The rotational axis of the dynamometer was aligned to the lateral femoral condyle of the leg.
Surface electromyography (EMG) (Twente Medical Systems International BV, Enschede, the Netherlands) recordings of the quadriceps (vastus medialis [VM] and vastus lateralis [VL]) and hamstring (biceps femoris [BF] and semitendinosus [ST]) muscles were made using pairs of surface electrodes (Ag/AgCl, inter-electrode distance=25 mm) that were attached to the skin after shaving and cleaning with alcohol. Electrode placement was done according to SENIAM (Surface Electromyography for the Noninvasive Assessment of Muscles) recommendations.36 Electromyographic data were recorded at a sampling rate of 1,000 Hz.
Procedure
First, a maximal strength test consisting of 3 maximal isometric knee extension contractions at 90 degrees of knee flexion (exertion time=5 seconds, recovery period=30 seconds) was performed.37 Peak torque was determined for each extension contraction, and the mean of these 3 peak torques was set as the maximal voluntary torque (100% MVT). For the normalization procedure of the EMG signals, maximal isometric knee flexion contractions were performed similarly to the maximal knee extension contractions (Fig. 1A).
Typical examples of the extension torque and electromyograpy (EMG) profiles of a selected agonist-antagonist pair during the different dynamometer tests in this study. (A) Three maximal isometric contractions at net extension torque (upper panel) and at normalized EMG amplitude (lower panel) of agonist vastus medialis muscle (VM) (dark gray line) and antagonist biceps femoris muscle (BF) (light gray line). The gray shaded bars indicate the phases over which CAI was calculated and averaged (ie, net joint torque is >50% of maximal voluntary contraction). (B) First 3 submaximal isotonic contractions (of a full series of 20 repetitions) at the low-load condition in knee extension (in degrees) (upper panel) and at normalized EMG amplitude (lower panel) of agonist VM (dark gray line) and antagonist BF (light gray line). The gray shaded bars indicate the phases over which CAI was calculated and averaged (ie, the dynamometer arm was pushed toward extension) to assess the effect of participant group and load level. (C) A full series (20 repetitions) of submaximal isotonic contractions until fatigue at the low-load condition in knee extension (in degrees) (upper panel) and at normalized EMG amplitude (lower panel) of agonist VM (dark gray line) and antagonist BF (light gray line). The gray shaded bars indicate the phases over which CAI was calculated (ie, the dynamometer arm was pushed toward extension). The change in CAI over the complete set of contractions was analyzed to assess the effect of fatigue.
Subsequently, a series of submaximal isotonic contractions were performed according to the protocol described by Eken et al.18 First, participants performed a warm-up and familiarization session of 15 knee extension contractions at a submaximal load of 20% MVT. Afterward, they performed 3 series of isotonic knee extension contractions against submaximal loads until exhaustion. The maximal number of extension contractions that participants were able to execute against each given load was measured and defined as the RM. Between submaximal tests, participants had a 5-minute rest period to recover from local fatigue.38 The series of repetitive submaximal contractions started at a fixed position of 90 degrees of knee flexion. Participants were instructed to slowly extend their knee until a range of motion of 40 degrees was reached, as indicated by a physical target (a stick) placed in front of the participant. Offline output of the dynamometer confirmed that angular velocity was around 60°/s for all participants. The series of submaximal contractions were performed at 3 load levels (low, medium, and high), ranging from 50% to 90% MVT. The percentages were imposed as such that the number of repetitions (RM) was 21 to 30 in the low-load condition, 10 to 20 in the medium-load condition, and below 10 in the high-load condition. The first test was performed at 70% MVT. The other 2 loads were selected depending on the number of repetitions executed on this test. If the participant executed ≥21 repetitions, the loads of the remaining 2 tests were set at 80% and 90% MVT to keep the number of anticipated repetitions below 25. If the participant executed ≤10 repetitions at 70% MVT, the loads of the remaining 2 tests were set at 50% and 60% MVT. If the participant executed between 10 and 20 repetitions at 70% MVT, the loads of the remaining 2 tests were set at 60% and 80% MVT. These remaining 2 tests were imposed in random order.
Data Analysis
Electromyographic recordings of the muscles during the maximal isometric and submaximal repetitions to fatigue (RTF) tests were processed offline using Matlab (version R2010b, The Mathworks Inc, Natick, Massachusetts). Movement artifacts were removed by high-pass filtering at 20 Hz.36 Additionally, EMG signals were rectified and low-pass filtered (second-order Butterworth filter, bidirectional at 5 Hz) to obtain smoothed, rectified EMG (SR-EMG) envelopes.39 Prior to calculating the coactivation index (CAI), SR-EMG tracings from the VM and VL were normalized to the maximal amplitude obtained during the maximal isometric knee extension contractions, and SR-EMG tracings from the BF and ST were normalized to those of the maximal isometric knee flexion contractions.40 Afterward, the CAI was calculated for the maximal isometric and submaximal RTF tests, according to the formula of Doorenbosch and Harlaar41:
in which EMGampagonist represents the normalized SR-EMG of the agonist muscle (knee extensors VM or VL), EMGampantagonist represents the normalized SR-EMG of the antagonist muscle (knee flexors BF or ST), i the sample number, and n is the total number of samples during the extension phase. A CAI value of 1 indicates complete coactivation, and a CAI value of 0 represents total absence of coactivation.
Figure 1 displays examples of the extension phases during which the CAI was calculated. The extension phase during the maximal isometric contractions included the samples during which the exerted torque was more than 50% MVT (Fig. 1A). The extension phase during the submaximal isotonic contractions included samples during which the range of motion moved from knee flexion to knee extension (Figs. 1B and 1C). The CAI was determined over these described extension phases. Subsequently, the CAI was averaged over 3 maximal isometric contractions to enhance accuracy (Fig. 1A). Similarly, the CAI was averaged over the first 3 consecutive submaximal contractions for each load condition (Fig. 1B). To assess the potential effect of fatigue, we calculated the CAI of each subsequent contraction separately for the low-, medium-, and high-load conditions (a typical example of the low-load condition is shown in Fig. 1C).
Statistical Analysis
Differences in demographic characteristics, such as age, height, weight, and body mass index, among the adolescents with TD, those with CP classified in GMFCS level I, and those with CP classified in GMFCS level II were analyzed using a one-way analysis of variance (ANOVA with post hoc Bonferroni correction). To test for differences in CAI values among the 3 groups during the maximal isometric contractions, a one-way ANOVA also was used. A 3 × 3 ANOVA for repeated measures was used to evaluate differences in CAI values among the 3 groups (between-subject factor) and among the 3 load levels (within-subject factor). To test whether changes in CAI values with increasing load were different among the groups, an overall group × load interaction was included. Maximal isometric and submaximal isotonic contractions were analyzed separately because of the different testing conditions.
Regression analysis, using a mixed linear model, was used to assess the influence of muscle fatigue on CAI. This method was used because it adjusts for the dependency of the repeated measures within individual participants. The CAI was used as the dependent variable, and repetition number was used as the independent variable, resulting in a regression coefficient reflecting the change in CAI per repetition. Analyses were done separately for the low-, medium-, and high-load conditions and for the 3 participant groups. A P value of <.05 was considered to be statistically significant. Analyses were performed with IBM SPSS version 20.0 (IBM Corp, Armonk, New York).
Results
Table 1 presents the participants' characteristics. Adolescents with TD were significantly taller than adolescents with CP classified in both GMFCS levels I and II. Analysis of body mass index reached borderline significance (P=.051), but post hoc tests revealed no differences among the participant groups.
Participant Characteristicsa
Following the procedure of imposing submaximal loads, an average load of 65% MVT (SD=10%) was imposed during the low-load condition, with an average RM of 24 (SD=3); an average load of 75% MVT (SD=9%) was imposed during the medium-load condition, with an average RM of 15 (SD=2); and an average load of 85% MVT (SD=9%) was imposed during the high-load condition, with an average RM of 6 (SD=2).
The CAI during maximal isometric contractions differed significantly among groups. Post hoc analyses indicated significantly higher CAI values of the VM-BF and VL-ST muscle pairs in adolescents with CP in GMFCS level II compared with adolescents with TD and significantly higher CAI values of the VM-ST muscle pair in adolescents with CP in GMFCS level II compared with adolescents with TD and adolescents with CP in GMFCS level I (Tab. 2, Fig. 2). Significant group effects on CAI (Tab. 2, Fig. 2) also were found for the submaximal contraction, showing that CAI was higher in adolescents with CP in GMFCS level II compared with adolescents with CP in GMFCS level I and adolescents with TD at low, medium, and high loads for the VM-BF, VM-ST, and VL-ST muscle pairs. Differences in CAI for the VL-BF muscle pair did not reach statistical significance. No influence of load level on CAI was observed in all muscle pairs (Tab. 2). In addition, no interaction effect of group by load was observed (Tab. 2).
Coactivation Index During Submaximal (Isotonic) and Maximal (Isometric) Contractions and Results of 3×3 Repeated-Measures ANOVAa
Box plots of the coactivation index of the agonist-antagonist pairs: (A) vastus medialis muscle (VM) vs biceps femoris muscle (BF), (B) VM vs semitendinosus muscle (ST), (C) vastus lateralis muscle (VL) vs BF, and (D) VL vs ST, separately for the submaximal isotonic test with the lowest load, medium load, and highest load and for the maximal isometric voluntary contraction (MVC) test. Significant differences between the groups are indicated with a double asterisk (**). The box plots show the following: box=interquartile range (IQR, 25th–75th percentiles, Q1–Q3); upper whisker=Q3+1.5IQR; lower whisker=Q1–1.5IQR; outliers are presented when the maximum or minimum data point falls outside the range of the whiskers (triangle=maximum outlier; diamond=minimum outlier). TD=adolescents with typical development, GMFCS I=adolescents with cerebral palsy in Gross Motor Function Classification System level I, GMFCS II=adolescents with cerebral palsy in Gross Motor Function Classification System level II.
The influence of muscle fatigue on CAI was assessed by constructing regression models, including CAI as a function of repetition, for all 3 load conditions and all 3 participant groups separately. Regression models showed that CAI in adolescents with TD decreased significantly as a function of repetition number during the submaximal test in the low-load condition in the VM-ST, VL-BF, and VL-ST muscle pairs, whereas no changes in CAI during this fatigue test were observed in adolescents with CP in GMFCS levels I and II (Tab. 3). No significant changes in CAI as function of repetition number were observed during the submaximal contractions at medium and high load in adolescents with TD or adolescents with CP in GMFCS levels I and II (Tab. 3).
Regression Coefficients for Mixed Linear Regression Models Describing the Change in CAI (95% CI) per Repetition Over Repetitive Submaximal Contractions at Different Load Conditionsa
Discussion
This study aimed to investigate the effects of GMFCS level, load level, and muscle fatigue on muscle coactivation in adolescents with CP in comparison with adolescents with TD during dynamometer strength tests. Coactivation levels appeared to be substantially higher in adolescents with CP classified in GMFCS level II than in those classified in GMFCS level I and adolescents with TD. In general, mean CAI values were 60% and 63% in adolescents with CP in GMFCS level II, 40% and 40% in adolescents with CP in GMFCS level I, and 35% and 30% in adolescents with TD for submaximal and maximal contractions, respectively. These findings are consistent with previous research,24,42,43 although these studies did not distinguish between different GMFCS levels when investigating coactivation levels in individuals with CP. The higher coactivation levels in adolescents with CP in GMFCS level II are likely caused by reduced selective motor control,44 which causes the antagonist muscles to contract more in synergy with the agonist muscles. These findings were similar for both maximal and submaximal strength tests and can lead to an underestimation of agonist muscle strength performed in GMFCS level II. This is an important finding to take into account when interpreting results from strength tests undertaken in clinical practice or research. Moreover, the interpretation of the potential effect of strength training programs might be affected. An increase in the net extension moment might then be the consequence of an increase in agonist muscle strength or a decrease in coactivation of the antagonist muscle, or both. No differences in coactivation were observed between adolescents with GMFCS in level I and adolescents with TD. This finding indicates that maximal and submaximal dynamometer strength tests for adolescents with CP classified in GMFCS level I are not influenced by coactivation and, therefore, that fewer concerns about underestimation of the agonist muscle strength are present for these individuals.
Results on the effect of load level revealed that coactivation did not differ for submaximal loads among the 3 participant groups, suggesting that the ratio between agonist and antagonist activation levels is similar for the different load levels. This finding is in line with previous findings in adults with TD, indicating that with increasing isometric knee extension force (10%–100% of maximum value), no significant change in hamstring muscle coactivation was observed.29 As coactivation level does not differ with load level, we conclude that there is no preference for a specific load level at which strength tests should be performed in clinical practice in adolescents with CP. It has to be noted, however, that relatively high submaximal loads (>65% MVT) were imposed in this study.
Our results showed that the CAI of all 4 muscle pairs remained constant during the submaximal fatigue tests at medium and high loads in both adolescents with CP and adolescents with TD. In contrast, the CAI decreased in the low-load condition in adolescents with TD in 3 of the 4 muscle pairs, whereas it remained constant in adolescents with CP. As demonstrated in previous work,18 the agonist EMG amplitude increased during these submaximal fatigue tests in both adolescents with CP and adolescents with TD as a consequence of muscle fatigue. Further inspection of the data in the current study revealed that in the medium- and high-load tests of the adolescents with TD and in all loads of the adolescents with CP, the antagonist EMG amplitude increased in parallel with agonist activity, resulting in constant CAI values. Only in the low-load condition of the TD group did the antagonist EMG amplitude not increase as a function of repetition, resulting in a decline in the CAI values over the course of the test.
Previous studies among adults with TD performing submaximal contractions also showed parallel increases in agonist and antagonist amplitude, and hence constant CAI values during fatigue,45–49 similar to our results for medium- and high-load conditions. In contrast, other studies showed a lack of increase in antagonist EMG amplitude in adults with TD,30,31,50 which would result in a decline in CAI with fatigue, similar to our observations in the low-load condition in the TD group. Moreau et al32 used maximal repetitive contraction to study the effect of fatigue on coactivation in children with CP and children with TD. They observed a parallel decrease in agonist and antagonist EMG activity in children with CP but not in children with TD. However, these changes in EMG response in maximal contractions are difficult to compare with those in submaximal contractions. Although, in general, agonist EMG amplitude increases with fatigue submaximal contractions (ie, reflecting an increase in activation to compensate for the reduced force output at the muscle level), decreases with fatigue in maximal contractions also have been observed in previous research,51 reflecting a decrease in central drive. The lack of consensus in the literature on the effect of fatigue on coactivation makes it difficult to interpret these findings in a conclusive way. Hence, the difference in coactivation with fatigue between our CP and TD groups cannot be easily explained or corroborated. Nevertheless, the observed difference seems to warrant some caution when investigating strength or endurance using a dynamometer test at low loads between adolescents with CP and those with TD. Differences in coactivation might account for differences in test results.
Although we investigated coactivation levels during different dynamometer tests in adolescents with CP in this study, the exact extent to which the antagonist muscles contribute to the net knee extension moment measured by the dynamometer and, therefore, the extent to which agonist muscle strength is underestimated remain unclear. To reveal separate agonist and antagonist contributions would require a method to estimate the actual individual muscle forces from EMG signals, which is challenging. Earlier studies showed EMG activity-to-force relationships to be nonlinear in nature.52,53 In addition, to our knowledge, the EMG activity-to-force relationship has not been investigated in individuals with CP. Hence, from our results, no quantitative statements can be made about the proportion of the antagonists working on the net knee extension moment in adolescents with CP and the magnitude of the underestimation of agonist strength. Future research is recommended to quantify the EMG-to-force relationship in individuals with CP and to quantify coactivation levels more precisely in this population.
A limitation of this study is that contraction mode differed between submaximal and maximal conditions, from isometric to isotonic. This difference in contraction mode was necessary for manipulating the submaximal load levels. Despite this difference in contraction mode, effects of group were similar in both maximal and submaximal strength tests, which strengthens our conclusions. Another limitation of this study is the method used to normalize the surface EMG signals to amplitudes recorded during the isometric maximal voluntary contraction, because earlier studies3,11,22 suggested that these types of contractions could not be reliably determined in the CP population. As a consequence of an invalid maximal voluntary contraction trial, muscle activity might be overestimated. This overestimation of muscle activity might lead to CAI values above 1, which was observed in one participant with CP classified in GMFCS level II. A possible explanation for this phenomenon might be that this individual was not able to produce a sufficient level of muscle activation during the maximal voluntary knee flexion contraction. The knee flexor muscles showed higher amplitude (ie, were more active) when performing as an antagonist in comparison with performing as an agonist during the maximal voluntary knee flexion contraction. Reduced selectivity was probably a problem in this participant, which might have caused an invalid maximal voluntary contraction trial. However, lack of selectivity also might be seen as the primary problem of coactivation. Therefore, this person was not left out of the analysis. In addition, although normalization of EMG amplitude in people with motor disabilities is a common drawback, it does provide an estimation of the neuromuscular effort invested for a given task.
In conclusion, this study showed that adolescents with CP classified in GMFCS level II have higher levels of muscle coactivation than adolescents with CP classified in GMFCS level I and adolescents with TD during different dynamometer tests. These results suggest that the level of muscle coactivation is dependent on the severity level of CP. On the other hand, coactivation was shown to be independent of load level and fatigue in both adolescents with CP and adolescents with TD. Coactivation did change during fatigue in adolescents with TD when tested at the low-load condition. The higher levels of coactivation in adolescents with CP in GMFCS level II may lead to an underestimation of agonist muscle strength and should be taken into account when interpreting the results of strength tests.
Footnotes
Ms Eken, Dr Dallmeijer, Dr Doorenbosch, and Dr Houdijk conceptualized and designed the study. Dr Becher and Dr Dekkers contributed to the design of the study. Ms Eken carried out data collection and analysis and drafted the manuscript. Dr Dallmeijer, Dr Doorenbosch, and Dr Houdijk provided fund procurement. Dr Dallmeijer, Dr Doorenbosch, Dr Houdijk, Dr Becher, and Dr Dekkers reviewed and revised the manuscript and approved the final manuscript as submitted. Ms Eken, Dr Becher, and Dr Dekkers provided study participants. The authors acknowledge all of the participating children and their parents for their cooperation in this study.
Ethical approval for this study was granted by the Medical Ethical Committee of VU University Medical Center, Amsterdam, the Netherlands.
No commercial party having a direct financial interest in the results of the research supporting this article has conferred or will confer a benefit on the authors or on any organization with which the authors are associated.
The results of this study were presented at the XXIIth Annual Meeting of the European Society for Movement Analysis in Adults and Children; October 1–4, 2014; Rome, Italy.
This study was supported by the grant from Revalidatiefonds (grant no. R2010142) and Johanna Kinder Fonds and Kinderfonds Adriaanstichting (grant no. 2011-044).
- Received October 20, 2014.
- Accepted February 14, 2016.
- © 2016 American Physical Therapy Association
References
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