http://informahealthcare.com/dre ISSN 0963-8288 print/ISSN 1464-5165 online Disabil Rehabil, Early Online: 1–6 ! 2014 Informa UK Ltd. DOI: 10.3109/09638288.2014.935492
RESEARCH PAPER
Does muscle size matter? The relationship between muscle size and strength in children with cerebral palsy Siobha´n L. Reid1, Christian A. Pitcher1, Sıˆan A. Williams1, Melissa K. Licari1, Jane P. Valentine2,3, Peter J. Shipman4, and Catherine M. Elliott2,3 Disabil Rehabil Downloaded from informahealthcare.com by University of Otago on 01/11/15 For personal use only.
1
School of Sport Science, Exercise and Health, The University of Western Australia, Perth, Australia, 2Department of Paediatric Rehabilitation, Princess Margaret Hospital, Perth, Australia, 3School of Paediatrics and Child Health, The University of Western Australia, Perth, Australia, and 4 Department of Diagnostic Imaging, Princess Margaret Hospital, Perth, Australia Abstract
Keywords
Purpose: To investigate the muscle size–strength relationship of the knee flexors and extensors in children with spastic cerebral palsy (CP) in relation to typically developing children (TD). Methods: Eighteen children with spastic Diplegia, Gross Motor Function Classification System I– III (mean 7 y 5 mo SD 1 y 7 mo) and 19 TD children (mean 7 y 6 mo SD 1 y 9 mo) participated. Muscle volume (MV) and anatomical cross-sectional area (aCSA) were assessed using MRI. Measures of peak torque (PT) and work of the knee flexors and extensors were assessed isometrically and isokinetically using a Biodex dynamometer, and normalised to bodymass (Bm). Results: Children with CP were weaker than their TD peers across all torque variables (p50.05). MV and aCSA of the knee flexors (MV: p ¼ 0.002; aCSA: p ¼ 0.000) and extensors (MV: p ¼ 0.003; aCSA: p50.0001) were smaller in children with CP. The relationship between muscle size and strength in children with CP was weaker than the TD children. The strongest relationship was between MV and isometric PT/Bm for TD children (r ¼ 0.77–0.84), and between MV and isokinetic work (r ¼ 0.70–0.72) for children with CP. Conclusions: Children with CP have smaller, weaker muscles than their TD peers. However, muscle size may only partially explain their decreased torque capacity. MV appears to be a better predictor of muscle work in children with CP than aCSA. This is an important area of research particularly in regard to treatment(s) that target muscle and strength in children with CP.
Cerebral palsy, children, muscle strength, muscle strength–size relationship, muscle volume History Received 2 October 2013 Revised 7 May 2014 Accepted 4 June 2014 Published online 3 July 2014
ä Implications for Rehabilitation
This research adds to the evidence that children with CP have smaller, weaker knee flexor and extensor muscles than their TD peers. However, unlike their TD peers, muscle size does not necessarily relate to muscle strength. The weak correlation between MRI-derived muscle volume and isometric peak torque suggests children with CP are underpowered relative to their muscle size. For children with CP, muscle volume appears to be the best predictor of isokinetic muscle torque output. Therefore, when assessing the capacity of a muscle, it appears preferable to measure total muscle volume and torque development through a range of motion (isokinetic strength).
Introduction Cerebral palsy (CP) is the most common physical disability in childhood [1]. Impairments present in individuals with CP include abnormal muscle tone, muscular weakness, muscular contracture and patterns of abnormal co-activation, all of which can result in functional limitations of both the lower and upper extremities [2,3]. As such, many children with CP have difficulty with
Address for correspondence: Asst/Prof. Siobha´n Reid, School of Sport Science, Exercise and Health (M408), University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia. Tel: +61 8 6488 8781. Fax: +61 8 6488 1039. E-mail: [email protected]
tasks such as propelling wheelchairs, walking independently, negotiating steps and many activities of daily living [4]. It is well known that children with CP have a significant deficiency in muscular strength [5]. Wiley and Damiano, in 1998, confirmed that children with CP were indeed weaker than their typically developing (TD) peers in all major muscle groups of the lower limb, and numerous studies have since confirmed this [6–9]. The maintenance of muscle strength in children with CP is important as a direct relationship exists between lower limb strength and gross motor function [5,10]. Yet, the neuromuscular and biomechanical basis for the observed weaknesses remains poorly understood. Clinically, it has long been assumed that the deficient strength was the result of spasticity. However, the origin of weakness is
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now thought to be due to a combination of agonist deficiency, alterations in neural drive and patterns of co-contraction [5,11–13]. Whilst the neural components are likely to contribute to the reported strength deficits, there is also evidence that spastic muscles show differences in structural morphology that may affect force generation capabilities [14–16]. Shortland [17] suggest that investigations into muscle morphology are required to further understand the deficits in strength displayed by children with CP. It is well documented that muscular strength is related to muscle size in the adult and adolescent population [18–20], and it is currently unknown if children with CP will demonstrate a similar relationship. Imaging modalities now allow the comparison of the muscle size–strength relationship in children with and without CP with relative ease. Magnetic resonance imaging (MRI) and improvements in strength assessment techniques have enabled greater accuracy in measurement, improving the evaluation of muscle size and strength [21,22]. MRI is currently the gold-standard measure for assessing muscle size in vivo, providing non-invasive imaging that avoids radiation exposure [23]. Comparisons of imaging techniques have demonstrated MRI to be superior to computer tomography and ultrasonography when analyzing structural morphology of soft tissues [24], thus permitting the highly accurate assessment of individual muscle morphology. Muscle physiological cross-sectional area (pCSA) is considered the most significant muscle size parameter relating to the maximal isometric force output of a muscle [25]. However, true pCSA requires the determination of muscle fiber length and pennation angle which cannot be determined easily in vivo [19] and can vary throughout the length of the muscle. Alternatively, MR imaging can be used to determine muscle volume (MV), and muscle anatomical cross sectional area (aCSA). Both aCSA and MV show a strong relationship with muscle peak force outputs and muscle peak torque outputs in adult populations [19,20]. Moreover, MR imaging estimates of MV and aCSA have been found to be reliable and valid measures when compared to anatomical measures obtained from cadaveric specimens [24]. Advancements in the assessment of muscle force output also assist our understanding of muscle performance. The use of isokinetic dynamometry has become increasingly popular in the study of children to assess the dynamic component of force output or ‘‘strength’’. Muscles function dynamically during everyday activities [26] and isokinetic dynamometry permits the assessment of dynamic muscle function through a range of motion at constant velocity [27], which is measured as torque about a joint and is expressed in Newton meters (Nm). Joint work is another useful way to understand muscle capacity during dynamic tasks, as it is the product of force and displacement and is measured in Joules (J). Joint work can be represented graphically by the area under the torque-joint position curve, and is therefore very useful in describing motion when torque can vary as a function of joint position. The evaluation of peak torque and joint work using isokinetic dynamometry may provide a better understanding of the dynamic muscle properties in specific muscle groups. The reliability of isokinetic strength assessment in pediatric populations has been established in numerous investigations [28,29], including children with cerebral palsy [30]. Using these techniques, Deighan et al. [29] added support for the size–strength relationship in a population of TD children, reporting strong correlations between isokinetic peak torque and MRI determined muscle aCSA for the knee extensors (r ¼ 0.86, p50.05) and flexors (r ¼ 0.83, p50.05) in children aged 9–10 years [29]. Furthermore, Pitcher et al. [31] reported that in TD children aged 5–11 years, MRI-derived MV was more highly correlated to measures of torque than aCSA.
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The current muscle morphology literature consistently demonstrates that children with CP display reduced muscle size compared to their TD peers [7,16,32]. However, none have examined the size–strength relationship in children with CP. Given that children with CP display pervasive muscle weakness across all muscle groups, it is important to understand the contribution of muscle morphology to the equation. With the ease of MR imaging and progress in the dynamic assessment of strength, the size–strength relationship can be established in children with CP. A detailed understanding of the relationship between muscle size and strength, may allow optimal selection and timing of muscle-targeted treatment(s) that could lead to improvements in the quality of life for children with CP. The aim of this study was to compare the strength and muscle size in TD children, with children who have spastic diplegia CP. We hypothesizse that: (1) The strength parameters (joint torque and work) of the knee flexors and extensors will be significantly lower in children with spastic diplegia when compared to their TD peers. (2) The aCSA and MV of knee flexors and extensors will be significantly lower in children with spastic diplegia compared to TD children. (3) The relationship between strength (joint torque and work) and muscle morphology (aCSA and MV) will be weaker in children with CP than TD children.
Methods Participants Eighteen participants with spastic diplegia (11 males, seven females; mean age 7 y 5 mo [SD 1 y 7mo], range 6–10 y) were recruited via the spasticity management service at Princess Margaret Hospital (PMH) in Perth, Australia. Participants were classified as Levels I to III on the Gross Motor Function Classification System (GMFCS) [33] and had bilateral lowerextremity involvement. Only ambulant children were recruited to minimize the effect of physical immobility on strength and muscle morphology. Seven children were classified as GMFCS Level I, nine as Level II, and two as Level III. Exclusion criteria included any history of orthopedic surgery or neurosurgery, and botulinum toxin injections within five months of testing. A convenient sample of 19 typically-developing children (nine males, 10 females; mean age 7 y 6 mo [SD1y 9mo], range 5–11 y) with no known neurological or orthopedic problems was also recruited. All parents or carers gave informed, written consent and participants provided assent. Ethical approval was obtained from the Human Research Ethics Committee at PMH (#1693) and The University of Western Australia (F5143), in accordance with the Helsinki Declaration of 1975. Procedures A Biodex System-3 dynamometer (Biodex Medical Systems, Inc., Shirley, NY) was employed to assess isometric and isokinetic strength of the knee flexors and extensors. Participants performed a set of warm-up exercises to familiarize themselves with the concentric muscle actions. Children performed three maximum unilateral isometric contractions, and three continuous maximum unilateral isokinetic (concentric/concentric) repetitions, of the knee flexors and extensors bilaterally. The order of action type and side-tested was randomized. Isometric trials evaluated peak torque (PT/Bm) in a static posture with the knee at 90 knee flexion. Isokinetic trials assessed peak torque (PT/Bm) and joint work (W/Bm) throughout range of motion at 60 /s.
Does muscle size matter?
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DOI: 10.3109/09638288.2014.935492
Subsequently, children completed a practice MR session to familiarize themselves with the scan procedure and to developed skills to enable them to lie still for a readable MR. Axial spinecho T1-weighted MR images were acquired of both legs simultaneously from the level of the ankle malleoli to the iliac crest while subjects lay prone in a 1.5 T whole body magnetic resonance unit (Magnetom Sonata Maestro Class, Seimens Medical Solutions, Erlangen, Germany). Subjects were positioned in neutral hip rotation, maintained passively using standard patient positioning with foam pads. Images in the thigh and lower legs were collected using a repetition time of 572 ms, echo time of 13 ms, slice thickness of 5 mm and mean inter-slice gap between 5 and 7 mm. A matrix size of 256 136 mm was used for all scans, and the field of view (280–300 mm) was varied to maximize in-plane resolution for each scan. The mean number of axial slices for the thigh was 27.7 (SD ¼ 0.5). The MR images were transferred to an independent workstation for digital reconstruction. Isotropic voxel size was obtained using a trilinear interpolation routine. Muscles were manually traced and segmented for all subjects using a digitization tablet (Intuos2, Wacom Technology Corp., Vancouver, WA) and Mimics software (Version 9.0, Materialise, Leuven). The six muscles segmented were the rectus femoris, vastus lateralis, vastus medialis, semitendinosus, biceps femoris and semimembranosus. Figure 1(A) illustrates a manually segmented slice from a TD participant and from a participant with CP. MV was calculated by summing the number of voxels contained within each muscle and multiplying by the voxel dimension (1 mm3), total MV was then determined as the sum of the individual knee flexor (semitendinousis, biceps femoris and semimembranosus) and extensor (rectus femoris, vastus lateralis, vastus medialis) muscle volumes. Calculation of aCSA was determined by the mean aCSA over three-slices exhibiting the greatest muscle area for each individual muscle, and summed to create total knee flexor and extensor aCSA. Statistical analysis Normal Q–Q plots demonstrated that all variables were normally distributed, therefore parametric statistics were employed. Group means were then calculated and independent t-tests were used to compare the groups (two-tailed, a-level ¼ 0.05). Pearson’s correlations were performed to investigate the relationship between muscle size (MV and aCSA) and isometric and isokinetic strength variables PT/Bm and work/Bm. Correlations were considered statistically significant at the 0.05 level.
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Results There were no significant differences in height (TD ¼ 128.2 cm [11.5]: CP ¼ 123.2 cm [10.2]) or body mass (TD ¼ 26.3 kg [6.1]: CP ¼ 23.7 kg [4.2]) between the two groups (p ¼ 0.18 and p ¼ 0.14, respectively), although the CP children tended to be shorter and lighter that TD children. Significant differences existed across all variables of muscle morphology and measures of strength between children with and without CP (Table 1). Children with CP display reduced MV of both the flexors (t ¼ 3.39, p ¼ 0.002, ES ¼ 1.14) and extensors (t ¼ 3.187, p ¼ 0.003, ES ¼ 1.06) compared to TD children. This represents a mean reduction of 29% for knee flexor and 25% in extensor MV compared to TD peers. Similarly, aCSA was significantly reduced in the flexors (t ¼ 9.73, p ¼ 0.000, ES ¼ 3.29) and extensors (t ¼ 8.49, p ¼ 0.000, ES ¼ 2.81) in children with CP. This represents a mean reduction of 54% in flexor and 49% extensor aCSA compared to TD peers. Children with CP demonstrated significant weakness across all measures of strength for both the knee flexors and extensors compared to TD children (Table 1). This equated to a reduced peak torque output at the knee flexors of 29% isometrically, 23% isokinetically and reduced joint work by 53% compared to TD children. Knee extensor peak torque output of children with CP was reduced by 26% isometrically, 20% isokinetically, and joint work was reduced by 33% compared to TD peers.
Table 1. Group differences in measures of knee muscle morphology and strength.
Variables 3
MV (cm ) aCSA (cm2) Isometric PT/Bm (Nm/kg) Isokinetic PT/Bm (Nm/kg) Joint Work/Bm (J/kg)
Muscle group Flexors Extensors Flexors Extensors Flexors Extensors Flexors Extensors Flexors Extensors
CP group (n ¼ 18) 127.3 287.9 6.6 12.9 65.4 186.8 67.2 135.2 44.0 109.2
(36.5) (76.1) (1.8) (4.0) (28.8) (43.0) (28.8) (38.9) (28.8) (38.8)
TD group (n ¼ 19)
p
178.7 (53.7) 382.2 (101.4) 14.2 (2.8) 25.3 (4.9) 91.8 (24.0) 250.8 (65.6) 87.7 (21.4) 168.1 (41.9) 93.2 (29.0) 162.8 (41.0)
0.002 0.003 50.000 50.000 0.005 0.001 0.019 0.018 50.000 50.000
Values displayed represent mean (±SD) (CP, cerebral palsy; TD, typically developing; MV, muscle volume; aCSA, anatomical cross-sectional area; PT, peak torque; Bm, body mass).
Figure 1. Bilateral axial slices of six manually outlined thigh muscles; VL, vastus lateralis; RF, rectus femoris; VM, vastus medialis; BF, biceps femoris; ST, semitendinosus; SM, semimembranosus. (A) represents a typically developing child and (B) represents a child with spastic diplegia CP.
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Table 2. Pearson’s correlations and Fisher’s Z scores between knee muscle morphology and strength in children with and without cerebral palsy.
Muscle group Isometric PT/Bm (Nm/kg) Isokinetic PT/Bm (Nm/kg) Joint Work/Bm (J/kg)
Flexors Extensors Flexors Extensors Flexors Extensors
MV in CP (n ¼ 18)
MV in TD (n ¼ 19)
Fisher Z MV
aCSA in CP (n ¼ 18)
aCSA in TD (n ¼ 19)
Fisher’s Z aCSA
0.54a 0.27 0.59a 0.51a 0.70b 0.72b
0.84b 0.77b 0.75b 0.67b 0.70b 0.72b
1.72* 2.01* 0.82 0.69 0.57 0.00
0.29 0.11 0.09 0.31 0.07 0.01
0.73b 0.71b 0.69b 0.62b 0.68b 0.68b
1.75* 2.16* 2.61y 2.91y 2.11* 2.28*
Significant correlation p50.05; bsignificant correlation p50.01; (MV, muscle volume; aCSA, anatomical cross-sectional area; CP, cerebral palsy; TD, typically developing; PT, peak torque; Bm, body mass); Fisher’s Z scores, assess the significant difference between two correlation coefficients; *p50.05, yp50.01.
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a
Figure 2. Relationship between MV and work/Bm for (A) the knee flexors and (B) the knee extensors in children with spastic diplegia cerebral palsy (CP) compared to typically-developing (TD) children.
As displayed in Table 2, TD children display strong significant relationships between all measures of strength and MV (r ¼ 0.67– 0.84). While slightly decreased compared to MV, aCSA also demonstrates strong significant correlations across all variables of muscle strength for TD children (r ¼ 0.62–0.73). The strongest relationship occurred between isometric PT/Bm and muscle size (MV r ¼ 0.84; aCSA r ¼ 0.73). However, aCSA demonstrates weak correlations to all measures of muscle strength in children with CP (r ¼ 0.31–0.29). Positive significant correlations were demonstrated between MV and all measures of muscle strength in children with CP (r ¼ 0.29–0.72). The strongest relationship was observed between MV and joint work for the knee flexors (r ¼ 0.70) and knee extensors (r ¼ 0.72) in children with CP. Fisher’s Z scores demonstrate significant differences between the relationship of MV and isometric PT/Bm in children with and without CP (Flexors Z ¼ 1.72; Extensors Z ¼ 2.01). However, no significant differences were evidenced in the correlations of isokinetic PT/Bm or Joint Work and MV between children with and without CP. All correlations between aCSA and each strength variable were significantly different between the two groups (Table 2). Figure 2 demonstrates the relationship between joint work and MV for the knee flexors and extensors in children with and without CP. In both cases, children with CP cluster at the lower end of the size–strength graphs. The strongest children with CP produce half the joint work capacity with half the MV of the strongest TD children.
Discussion The bigger a muscle is the greater its capacity for force generation [18], this relationship is known as the muscle size–strength relationship. The legitimacy of the muscle size–strength relationship has been demonstrated time and again in unimpaired adults [19], adolescents [21] and more recently in TD children [31].
This research aimed to determine the nature of the muscle size–strength relationship in children with spastic type CP. Children with CP demonstrated significant decrements across all measures of strength compared to their TD peers. Although no differences were evident in height and weight between the groups, the torque output of children with CP was consistently 20–30% less than the TD children, supporting the first hypothesis. These results are consistent with previous literature documenting significant muscle weakness in children with CP [2,4,5,34]. Although all the children with CP were a highly functional group of children classified as GMFCS I–III, the results indicate strength discrepancies between the two groups, this was more evident at the knee flexors than the knee extensors. Moreover, children with CP could produce only half the knee flexor work output of the TD children. Not only were the muscles of children with CP weaker, but they were also significantly smaller. Children with CP displayed approximately 70–75% MV of their TD peers, whereas their aCSA was reduced to as little as 55% of their TD peers. This data is consistent with previous reports of diminished muscle size in children using ultrasound [32,35] and MRI [7,16,17]. However, no previous reports have matched the size of children’s muscles with their strength capacity, to document the size–strength relationship in children with CP. We have asked the question: could the reduction in torque production be related to muscle size? In TD children, both morphological measures of MV and aCSA demonstrate strong significant relationships to all variables of strength; this is consistent with the adult and adolescent literature [21]. Furthermore, these correlations (established via MRI) are higher than those reported previously in children using ultrasonography [36]. A strong relationship between muscle size and strength was not evident for children with CP, supporting the third hypothesis. MV demonstrated a weaker correlation to torque
Does muscle size matter?
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DOI: 10.3109/09638288.2014.935492
in children with CP; however, no correlation could be established between aCSA and any measure of strength in this population. Moreover, Fisher’s Z scores revealed there was a significant difference in the aCSA size–strength relationships between the groups, children with CP consistently demonstrated poorer aCSA size–strength relationships. It is conceivable that MV is a better indicator of growth and development; therefore, a better predictor of the ‘‘strength health’’ of a muscle. As MV is the product of physiological CSA and fiber length, and joint torque is directly affected by both force and length [37], it is likely to be particularly useful in understanding the size–strength relationship in pediatric populations. It is therefore recommended that measurements of muscle morphology in children should include estimates of volume to best represent the capacity of the muscle, particularly when measures of the physiological CSA are unattainable. It is generally accepted that a muscle demonstrates increased force generating capacity during isometric contractions than during concentric contractions [38]. This principle was demonstrated by the TD children, as the greatest size–strength relationship existed between measures of morphology (MV and aCSA) and isometric PT/Bm. However, the strength profiles of children with CP did not follow this principle, demonstrating weak to moderate correlations between MV and isometric PT/Bm. These observations suggest that the muscles of children with CP are not only under-sized but under-powered with respect to producing isometric torque, relative to their muscle size. Although in the present study we did not assess motor unit activation, it appears that deficiencies in neuromotor functioning may partly explain the significant reduction in isometric torque output relative to muscle size; however, they do not appear to be the sole explanation. Whilst children with CP did not conform to the size–strength principle isometrically, they did demonstrate a very interesting size–strength relationship in terms of joint work output. The strongest size–strength relationship existed between MV and joint work output for children with CP. Joint work (j/Bm) is the ability of a muscle(s), via a joint, to produce torque throughout range of motion, and represents the mechanical integrity of the muscle to operate dynamically. These results have demonstrated that children with CP have a significantly diminished capacity to produce work with respect to their TD peers. Such a decrement in a muscles’ capacity to do work may be detrimental to functional performance. However, joint work appears to be the best predictor of muscle morphology in CP, with Pearson’s r values equivalent to the TD population. Therefore, unlike isometric Pt/Bm, the assessment of joint work relative to MV does not appear to be influenced by alterations in neural drive, and may be a better indicator of muscle performance. Increased research attention should be paid to joint work capacity as a potential indicator of muscle health of children with CP.
Conclusions Children with CP have smaller, weaker muscles than their TD peers. However, the size of muscle does not necessarily relate to muscle strength outputs in children with CP. MV appears to be a better predictor of muscle strength than aCSA, and the greatest size–strength relationship exists between MV and joint work output. The weak correlation between MV and isometric PT/Bm suggests children with CP are under-powered relative to their muscle size. Further research is required to elucidate the nature of the size–strength imbalance. Altered neural drive appears to disturb the aCSA size–strength relationship. However, reduced capacity to do work at the joint appears to be more directly related to alterations in muscle volume. This area of research is likely to improve the efficacy of the assessment of muscle strength and
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morphology, and in turn improve treatments that target muscle functioning in children with CP.
Acknowledgements The authors would like to thank Professor Eve Blair for her assistance with the formulation of this manuscript, the Department of Paediatric Rehabilitation, Princess Margaret Hospital (PMH) for their support and assistance with recruitment and the Department of Diagnostic Imaging, PMH, in particular, Alex Kuenzel, for their assistance in data collection. Authors would also like to acknowledge the contribution of the School of Sport Science, Exercise & Health at UWA for the use of equipment and facilities.
Declaration of interest The authors report no conflicts responsible for the content and This project was supported Fellowship and the University and Development Awards.
of interest. The authors alone are writing of this article. by The Raine Medical Research of Western Australia’s Research
References 1. Reddihough DS, Collins KJ. The epidemiology and causes of cerebral palsy. Aust J Physiother 2003;49:7–12. 2. MacPhail H, Kramer J. Effect of isokinetic strength training on functional ability and walking efficiency in adolescents with cerebral palsy. Dev Med Child Neurol 1995;37:763–75. 3. Mayston MJ. People with cerebral palsy: effects of and perspectives for therapy. Neural Plasticity 2001;8:51–69. 4. Dodd KJ, Taylor NF, Damiano DL. A systematic review of the effectiveness of strength-training programs for people with cerebral palsy. Arch Phys Med Rehabil 2002;83:1157–64. 5. Wiley ME, Damiano DL. Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol 1998;40:100–7. 6. Damiano DL, Vaughan CL, Abel MF. Muscle response to heavy resistance exercise in children with spastic cerebral palsy. Dev Med Child Neurol 1995;37:731–9. 7. Elder GCB, Kirk J, Stewart G, et al. Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol 2003;45:542–50. 8. Stackhouse SK, Binder-Macleod SA, Lee SCK. Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 2005;31:594–601. 9. Reid S, Hamer P, Alderson J, Lloyd D. Neuromuscular adaptations to eccentric strength training for adolescents. Dev Med Child Neurol 2010;52:358–63. 10. Damiano D, Arnold A, Steele K, Delp S. Can strength training predictably improve gait kinematics? A pilot study on the effects of hip and knee extensor strengthening on lower extremity alignment in children with cerebral palsy. Phys Ther 2010;90:269–79. 11. Ross SA, Engsberg JR. Relation between spasticity and strength in individuals with spastic diplegic cerebral palsy. Development Med Child Neurol 2002;44:148–57. 12. Rose J, McGill KC. The motor unit in cerebral palsy. Dev Med Child Neurol 1998;40:270–7. 13. Brown JK, Rodda J, Walsh EG, Wright GW. Neurophysiology of lower-limb function in hemiplegic children. Dev Med Child Neurol 1991;33:1037–47. 14. Booth CM, Cortina-Borja MJF, Theologis TN. Collagen accumulation in muscle of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol 2001;43:314–20. 15. Lieber RL, Steinman S, Barash IA, Chambers H. Structural and functional changes in spastic skeletal muscle. Muscle Nerve 2004; 29:615–27. 16. Noble JJ, Fry N, Lewis A, et al. Lower limb muscle volumes in bilateral cerebral palsy. Brain Develop 2014;34:294–300. 17. Shortland A. Muscle deficits in cerebral palsy and early loss of mobility: can we learn something from our elders? Dev Med Child Neurol 2009;51:59–63. 18. Lieber RL, Fride´n J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 2000;23:1647–66.
Disabil Rehabil Downloaded from informahealthcare.com by University of Otago on 01/11/15 For personal use only.
6
S. L. Reid et al.
19. Bamman M, Newcomer B, Larson-Meyer D, et al. Evaluation of the strength-size relationship in vivo using various muscle size indices. Med Sci Sport Exer 2000;32:1307–13. 20. Akagi R, Takai Y, Ohia M, Kanehisa H. Muscle volume compared to cross-sectional area is more appropriate for evaluating muscle strength in young and elderly individuals. Age Ageing 2009;38:1–6. 21. Deighan M, De Ste Croix M, Armstrong N. Measurement of maximal muscle cross-sectional area of knee and elbow extensors and flexors in children, teenagers and adults. J Sports Sci 2006;24: 543–6. 22. Wood LE, Dixon S, Grant C, Armstrong N. Elbow flexion and extension strength relative to body size or muscle size in children. Med Sci Sport Exer 2004;36:1977–84. 23. Voronov A. Anatomical cross-sectional areas and volumes of the muscles of the lower extremities. Human Physiol 2003;29: 201–11. 24. Engstrom C, Loeb G, Reid J, et al. Morphometry of the human thigh muscles. A comparison between anatomical sections and computer tomographic and magnetic resonance images. J Anatomy 1990;176: 139–56. 25. Roy R, Edgerton VIKP. Skeletal muscle architecture and performance. In Komi P, ed. Strength and power in sport. Cambridge: Blackwell Scientific; 1992:115–29. 26. Beunen G, Thomis M. Muscular strength development in children and adolescents. Pediatr Exer Sci 2000;12:174–97. 27. Drouin J, Valovich M. Reliability and validity of the Biodex system 3 pro isokinetic dynamometer velocity, torque and position measurements. J Appl Physiol 2004;91:22–9. 28. De Ste Croix M, Deighan M, Armstrong A. Assessment and interpretation of isokinetic muscle strength during growth and maturation. Sports Med 2003;33:727–43.
Disabil Rehabil, Early Online: 1–6
29. Deighan M, De Ste Croix M, Armstrong N. Reliability of isokinetic knee and elbow strength in 9/10 year old boys. Isokinet Exer Sci 2003;11:209–15. 30. Ayalon M, Ben-Sira D, Hutzler Y, Gilad T. Reliabilty of isokinetic strength measuerment of the knee in children with cerebral palsy. Dev Med Child Neurol 2000;42:398–402. 31. Pitcher C, Elliott C, Williams S, et al. Childhood muscle morphology and strength: alterations over six months of growth. Muscle Nerve 2012;46:360–6. 32. Moreau NG, Teefey SA, Damiano DL. In vivo muscle architecture and size of the rectus femoris and vastus lateralis in children and adolescents with cerebral palsy. Dev Med Child Neurol 2009;51: 800–6. 33. Palisano R, Rosenbaum P, Walter S, et al. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997;39:214–23. 34. Reid S, Hamer P, Alderson J, Lloyd D. Neuromuscular adaptations to eccentric strength training in children and adolescents with cererbal palsy. Dev Med Child Neurol 2010;52:358–63. 35. McNee AE, Gough M, Morrissey MC, Shortland AP. Increases in muscle volume after plantarflexor strength training in children with spastic cerebral palsy. Dev Med Child Neurol 2009; 51:429–35. 36. Kanehisa H, Yata H, Ikegawa S, Fukunaga T. A cross-sectional study of the size and strength of the lower leg muscles during growth. Eur J Appl Physiol 1995;72:150–6. 37. Fukunaga T, Kubo K, Kawakami Y, et al. In vivo behaviour of human muscle tendon during walking. Proc Royal Soc Lond 2001; 268:229–33. 38. Enoka RM. Neuromechanics of human movement. 3rd ed. Champaign (IL): Human Kinetics; 2002.
RESEARCH PAPER
Does muscle size matter? The relationship between muscle size and strength in children with cerebral palsy Siobha´n L. Reid1, Christian A. Pitcher1, Sıˆan A. Williams1, Melissa K. Licari1, Jane P. Valentine2,3, Peter J. Shipman4, and Catherine M. Elliott2,3 Disabil Rehabil Downloaded from informahealthcare.com by University of Otago on 01/11/15 For personal use only.
1
School of Sport Science, Exercise and Health, The University of Western Australia, Perth, Australia, 2Department of Paediatric Rehabilitation, Princess Margaret Hospital, Perth, Australia, 3School of Paediatrics and Child Health, The University of Western Australia, Perth, Australia, and 4 Department of Diagnostic Imaging, Princess Margaret Hospital, Perth, Australia Abstract
Keywords
Purpose: To investigate the muscle size–strength relationship of the knee flexors and extensors in children with spastic cerebral palsy (CP) in relation to typically developing children (TD). Methods: Eighteen children with spastic Diplegia, Gross Motor Function Classification System I– III (mean 7 y 5 mo SD 1 y 7 mo) and 19 TD children (mean 7 y 6 mo SD 1 y 9 mo) participated. Muscle volume (MV) and anatomical cross-sectional area (aCSA) were assessed using MRI. Measures of peak torque (PT) and work of the knee flexors and extensors were assessed isometrically and isokinetically using a Biodex dynamometer, and normalised to bodymass (Bm). Results: Children with CP were weaker than their TD peers across all torque variables (p50.05). MV and aCSA of the knee flexors (MV: p ¼ 0.002; aCSA: p ¼ 0.000) and extensors (MV: p ¼ 0.003; aCSA: p50.0001) were smaller in children with CP. The relationship between muscle size and strength in children with CP was weaker than the TD children. The strongest relationship was between MV and isometric PT/Bm for TD children (r ¼ 0.77–0.84), and between MV and isokinetic work (r ¼ 0.70–0.72) for children with CP. Conclusions: Children with CP have smaller, weaker muscles than their TD peers. However, muscle size may only partially explain their decreased torque capacity. MV appears to be a better predictor of muscle work in children with CP than aCSA. This is an important area of research particularly in regard to treatment(s) that target muscle and strength in children with CP.
Cerebral palsy, children, muscle strength, muscle strength–size relationship, muscle volume History Received 2 October 2013 Revised 7 May 2014 Accepted 4 June 2014 Published online 3 July 2014
ä Implications for Rehabilitation
This research adds to the evidence that children with CP have smaller, weaker knee flexor and extensor muscles than their TD peers. However, unlike their TD peers, muscle size does not necessarily relate to muscle strength. The weak correlation between MRI-derived muscle volume and isometric peak torque suggests children with CP are underpowered relative to their muscle size. For children with CP, muscle volume appears to be the best predictor of isokinetic muscle torque output. Therefore, when assessing the capacity of a muscle, it appears preferable to measure total muscle volume and torque development through a range of motion (isokinetic strength).
Introduction Cerebral palsy (CP) is the most common physical disability in childhood [1]. Impairments present in individuals with CP include abnormal muscle tone, muscular weakness, muscular contracture and patterns of abnormal co-activation, all of which can result in functional limitations of both the lower and upper extremities [2,3]. As such, many children with CP have difficulty with
Address for correspondence: Asst/Prof. Siobha´n Reid, School of Sport Science, Exercise and Health (M408), University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia. Tel: +61 8 6488 8781. Fax: +61 8 6488 1039. E-mail: [email protected]
tasks such as propelling wheelchairs, walking independently, negotiating steps and many activities of daily living [4]. It is well known that children with CP have a significant deficiency in muscular strength [5]. Wiley and Damiano, in 1998, confirmed that children with CP were indeed weaker than their typically developing (TD) peers in all major muscle groups of the lower limb, and numerous studies have since confirmed this [6–9]. The maintenance of muscle strength in children with CP is important as a direct relationship exists between lower limb strength and gross motor function [5,10]. Yet, the neuromuscular and biomechanical basis for the observed weaknesses remains poorly understood. Clinically, it has long been assumed that the deficient strength was the result of spasticity. However, the origin of weakness is
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now thought to be due to a combination of agonist deficiency, alterations in neural drive and patterns of co-contraction [5,11–13]. Whilst the neural components are likely to contribute to the reported strength deficits, there is also evidence that spastic muscles show differences in structural morphology that may affect force generation capabilities [14–16]. Shortland [17] suggest that investigations into muscle morphology are required to further understand the deficits in strength displayed by children with CP. It is well documented that muscular strength is related to muscle size in the adult and adolescent population [18–20], and it is currently unknown if children with CP will demonstrate a similar relationship. Imaging modalities now allow the comparison of the muscle size–strength relationship in children with and without CP with relative ease. Magnetic resonance imaging (MRI) and improvements in strength assessment techniques have enabled greater accuracy in measurement, improving the evaluation of muscle size and strength [21,22]. MRI is currently the gold-standard measure for assessing muscle size in vivo, providing non-invasive imaging that avoids radiation exposure [23]. Comparisons of imaging techniques have demonstrated MRI to be superior to computer tomography and ultrasonography when analyzing structural morphology of soft tissues [24], thus permitting the highly accurate assessment of individual muscle morphology. Muscle physiological cross-sectional area (pCSA) is considered the most significant muscle size parameter relating to the maximal isometric force output of a muscle [25]. However, true pCSA requires the determination of muscle fiber length and pennation angle which cannot be determined easily in vivo [19] and can vary throughout the length of the muscle. Alternatively, MR imaging can be used to determine muscle volume (MV), and muscle anatomical cross sectional area (aCSA). Both aCSA and MV show a strong relationship with muscle peak force outputs and muscle peak torque outputs in adult populations [19,20]. Moreover, MR imaging estimates of MV and aCSA have been found to be reliable and valid measures when compared to anatomical measures obtained from cadaveric specimens [24]. Advancements in the assessment of muscle force output also assist our understanding of muscle performance. The use of isokinetic dynamometry has become increasingly popular in the study of children to assess the dynamic component of force output or ‘‘strength’’. Muscles function dynamically during everyday activities [26] and isokinetic dynamometry permits the assessment of dynamic muscle function through a range of motion at constant velocity [27], which is measured as torque about a joint and is expressed in Newton meters (Nm). Joint work is another useful way to understand muscle capacity during dynamic tasks, as it is the product of force and displacement and is measured in Joules (J). Joint work can be represented graphically by the area under the torque-joint position curve, and is therefore very useful in describing motion when torque can vary as a function of joint position. The evaluation of peak torque and joint work using isokinetic dynamometry may provide a better understanding of the dynamic muscle properties in specific muscle groups. The reliability of isokinetic strength assessment in pediatric populations has been established in numerous investigations [28,29], including children with cerebral palsy [30]. Using these techniques, Deighan et al. [29] added support for the size–strength relationship in a population of TD children, reporting strong correlations between isokinetic peak torque and MRI determined muscle aCSA for the knee extensors (r ¼ 0.86, p50.05) and flexors (r ¼ 0.83, p50.05) in children aged 9–10 years [29]. Furthermore, Pitcher et al. [31] reported that in TD children aged 5–11 years, MRI-derived MV was more highly correlated to measures of torque than aCSA.
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The current muscle morphology literature consistently demonstrates that children with CP display reduced muscle size compared to their TD peers [7,16,32]. However, none have examined the size–strength relationship in children with CP. Given that children with CP display pervasive muscle weakness across all muscle groups, it is important to understand the contribution of muscle morphology to the equation. With the ease of MR imaging and progress in the dynamic assessment of strength, the size–strength relationship can be established in children with CP. A detailed understanding of the relationship between muscle size and strength, may allow optimal selection and timing of muscle-targeted treatment(s) that could lead to improvements in the quality of life for children with CP. The aim of this study was to compare the strength and muscle size in TD children, with children who have spastic diplegia CP. We hypothesizse that: (1) The strength parameters (joint torque and work) of the knee flexors and extensors will be significantly lower in children with spastic diplegia when compared to their TD peers. (2) The aCSA and MV of knee flexors and extensors will be significantly lower in children with spastic diplegia compared to TD children. (3) The relationship between strength (joint torque and work) and muscle morphology (aCSA and MV) will be weaker in children with CP than TD children.
Methods Participants Eighteen participants with spastic diplegia (11 males, seven females; mean age 7 y 5 mo [SD 1 y 7mo], range 6–10 y) were recruited via the spasticity management service at Princess Margaret Hospital (PMH) in Perth, Australia. Participants were classified as Levels I to III on the Gross Motor Function Classification System (GMFCS) [33] and had bilateral lowerextremity involvement. Only ambulant children were recruited to minimize the effect of physical immobility on strength and muscle morphology. Seven children were classified as GMFCS Level I, nine as Level II, and two as Level III. Exclusion criteria included any history of orthopedic surgery or neurosurgery, and botulinum toxin injections within five months of testing. A convenient sample of 19 typically-developing children (nine males, 10 females; mean age 7 y 6 mo [SD1y 9mo], range 5–11 y) with no known neurological or orthopedic problems was also recruited. All parents or carers gave informed, written consent and participants provided assent. Ethical approval was obtained from the Human Research Ethics Committee at PMH (#1693) and The University of Western Australia (F5143), in accordance with the Helsinki Declaration of 1975. Procedures A Biodex System-3 dynamometer (Biodex Medical Systems, Inc., Shirley, NY) was employed to assess isometric and isokinetic strength of the knee flexors and extensors. Participants performed a set of warm-up exercises to familiarize themselves with the concentric muscle actions. Children performed three maximum unilateral isometric contractions, and three continuous maximum unilateral isokinetic (concentric/concentric) repetitions, of the knee flexors and extensors bilaterally. The order of action type and side-tested was randomized. Isometric trials evaluated peak torque (PT/Bm) in a static posture with the knee at 90 knee flexion. Isokinetic trials assessed peak torque (PT/Bm) and joint work (W/Bm) throughout range of motion at 60 /s.
Does muscle size matter?
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DOI: 10.3109/09638288.2014.935492
Subsequently, children completed a practice MR session to familiarize themselves with the scan procedure and to developed skills to enable them to lie still for a readable MR. Axial spinecho T1-weighted MR images were acquired of both legs simultaneously from the level of the ankle malleoli to the iliac crest while subjects lay prone in a 1.5 T whole body magnetic resonance unit (Magnetom Sonata Maestro Class, Seimens Medical Solutions, Erlangen, Germany). Subjects were positioned in neutral hip rotation, maintained passively using standard patient positioning with foam pads. Images in the thigh and lower legs were collected using a repetition time of 572 ms, echo time of 13 ms, slice thickness of 5 mm and mean inter-slice gap between 5 and 7 mm. A matrix size of 256 136 mm was used for all scans, and the field of view (280–300 mm) was varied to maximize in-plane resolution for each scan. The mean number of axial slices for the thigh was 27.7 (SD ¼ 0.5). The MR images were transferred to an independent workstation for digital reconstruction. Isotropic voxel size was obtained using a trilinear interpolation routine. Muscles were manually traced and segmented for all subjects using a digitization tablet (Intuos2, Wacom Technology Corp., Vancouver, WA) and Mimics software (Version 9.0, Materialise, Leuven). The six muscles segmented were the rectus femoris, vastus lateralis, vastus medialis, semitendinosus, biceps femoris and semimembranosus. Figure 1(A) illustrates a manually segmented slice from a TD participant and from a participant with CP. MV was calculated by summing the number of voxels contained within each muscle and multiplying by the voxel dimension (1 mm3), total MV was then determined as the sum of the individual knee flexor (semitendinousis, biceps femoris and semimembranosus) and extensor (rectus femoris, vastus lateralis, vastus medialis) muscle volumes. Calculation of aCSA was determined by the mean aCSA over three-slices exhibiting the greatest muscle area for each individual muscle, and summed to create total knee flexor and extensor aCSA. Statistical analysis Normal Q–Q plots demonstrated that all variables were normally distributed, therefore parametric statistics were employed. Group means were then calculated and independent t-tests were used to compare the groups (two-tailed, a-level ¼ 0.05). Pearson’s correlations were performed to investigate the relationship between muscle size (MV and aCSA) and isometric and isokinetic strength variables PT/Bm and work/Bm. Correlations were considered statistically significant at the 0.05 level.
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Results There were no significant differences in height (TD ¼ 128.2 cm [11.5]: CP ¼ 123.2 cm [10.2]) or body mass (TD ¼ 26.3 kg [6.1]: CP ¼ 23.7 kg [4.2]) between the two groups (p ¼ 0.18 and p ¼ 0.14, respectively), although the CP children tended to be shorter and lighter that TD children. Significant differences existed across all variables of muscle morphology and measures of strength between children with and without CP (Table 1). Children with CP display reduced MV of both the flexors (t ¼ 3.39, p ¼ 0.002, ES ¼ 1.14) and extensors (t ¼ 3.187, p ¼ 0.003, ES ¼ 1.06) compared to TD children. This represents a mean reduction of 29% for knee flexor and 25% in extensor MV compared to TD peers. Similarly, aCSA was significantly reduced in the flexors (t ¼ 9.73, p ¼ 0.000, ES ¼ 3.29) and extensors (t ¼ 8.49, p ¼ 0.000, ES ¼ 2.81) in children with CP. This represents a mean reduction of 54% in flexor and 49% extensor aCSA compared to TD peers. Children with CP demonstrated significant weakness across all measures of strength for both the knee flexors and extensors compared to TD children (Table 1). This equated to a reduced peak torque output at the knee flexors of 29% isometrically, 23% isokinetically and reduced joint work by 53% compared to TD children. Knee extensor peak torque output of children with CP was reduced by 26% isometrically, 20% isokinetically, and joint work was reduced by 33% compared to TD peers.
Table 1. Group differences in measures of knee muscle morphology and strength.
Variables 3
MV (cm ) aCSA (cm2) Isometric PT/Bm (Nm/kg) Isokinetic PT/Bm (Nm/kg) Joint Work/Bm (J/kg)
Muscle group Flexors Extensors Flexors Extensors Flexors Extensors Flexors Extensors Flexors Extensors
CP group (n ¼ 18) 127.3 287.9 6.6 12.9 65.4 186.8 67.2 135.2 44.0 109.2
(36.5) (76.1) (1.8) (4.0) (28.8) (43.0) (28.8) (38.9) (28.8) (38.8)
TD group (n ¼ 19)
p
178.7 (53.7) 382.2 (101.4) 14.2 (2.8) 25.3 (4.9) 91.8 (24.0) 250.8 (65.6) 87.7 (21.4) 168.1 (41.9) 93.2 (29.0) 162.8 (41.0)
0.002 0.003 50.000 50.000 0.005 0.001 0.019 0.018 50.000 50.000
Values displayed represent mean (±SD) (CP, cerebral palsy; TD, typically developing; MV, muscle volume; aCSA, anatomical cross-sectional area; PT, peak torque; Bm, body mass).
Figure 1. Bilateral axial slices of six manually outlined thigh muscles; VL, vastus lateralis; RF, rectus femoris; VM, vastus medialis; BF, biceps femoris; ST, semitendinosus; SM, semimembranosus. (A) represents a typically developing child and (B) represents a child with spastic diplegia CP.
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Table 2. Pearson’s correlations and Fisher’s Z scores between knee muscle morphology and strength in children with and without cerebral palsy.
Muscle group Isometric PT/Bm (Nm/kg) Isokinetic PT/Bm (Nm/kg) Joint Work/Bm (J/kg)
Flexors Extensors Flexors Extensors Flexors Extensors
MV in CP (n ¼ 18)
MV in TD (n ¼ 19)
Fisher Z MV
aCSA in CP (n ¼ 18)
aCSA in TD (n ¼ 19)
Fisher’s Z aCSA
0.54a 0.27 0.59a 0.51a 0.70b 0.72b
0.84b 0.77b 0.75b 0.67b 0.70b 0.72b
1.72* 2.01* 0.82 0.69 0.57 0.00
0.29 0.11 0.09 0.31 0.07 0.01
0.73b 0.71b 0.69b 0.62b 0.68b 0.68b
1.75* 2.16* 2.61y 2.91y 2.11* 2.28*
Significant correlation p50.05; bsignificant correlation p50.01; (MV, muscle volume; aCSA, anatomical cross-sectional area; CP, cerebral palsy; TD, typically developing; PT, peak torque; Bm, body mass); Fisher’s Z scores, assess the significant difference between two correlation coefficients; *p50.05, yp50.01.
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a
Figure 2. Relationship between MV and work/Bm for (A) the knee flexors and (B) the knee extensors in children with spastic diplegia cerebral palsy (CP) compared to typically-developing (TD) children.
As displayed in Table 2, TD children display strong significant relationships between all measures of strength and MV (r ¼ 0.67– 0.84). While slightly decreased compared to MV, aCSA also demonstrates strong significant correlations across all variables of muscle strength for TD children (r ¼ 0.62–0.73). The strongest relationship occurred between isometric PT/Bm and muscle size (MV r ¼ 0.84; aCSA r ¼ 0.73). However, aCSA demonstrates weak correlations to all measures of muscle strength in children with CP (r ¼ 0.31–0.29). Positive significant correlations were demonstrated between MV and all measures of muscle strength in children with CP (r ¼ 0.29–0.72). The strongest relationship was observed between MV and joint work for the knee flexors (r ¼ 0.70) and knee extensors (r ¼ 0.72) in children with CP. Fisher’s Z scores demonstrate significant differences between the relationship of MV and isometric PT/Bm in children with and without CP (Flexors Z ¼ 1.72; Extensors Z ¼ 2.01). However, no significant differences were evidenced in the correlations of isokinetic PT/Bm or Joint Work and MV between children with and without CP. All correlations between aCSA and each strength variable were significantly different between the two groups (Table 2). Figure 2 demonstrates the relationship between joint work and MV for the knee flexors and extensors in children with and without CP. In both cases, children with CP cluster at the lower end of the size–strength graphs. The strongest children with CP produce half the joint work capacity with half the MV of the strongest TD children.
Discussion The bigger a muscle is the greater its capacity for force generation [18], this relationship is known as the muscle size–strength relationship. The legitimacy of the muscle size–strength relationship has been demonstrated time and again in unimpaired adults [19], adolescents [21] and more recently in TD children [31].
This research aimed to determine the nature of the muscle size–strength relationship in children with spastic type CP. Children with CP demonstrated significant decrements across all measures of strength compared to their TD peers. Although no differences were evident in height and weight between the groups, the torque output of children with CP was consistently 20–30% less than the TD children, supporting the first hypothesis. These results are consistent with previous literature documenting significant muscle weakness in children with CP [2,4,5,34]. Although all the children with CP were a highly functional group of children classified as GMFCS I–III, the results indicate strength discrepancies between the two groups, this was more evident at the knee flexors than the knee extensors. Moreover, children with CP could produce only half the knee flexor work output of the TD children. Not only were the muscles of children with CP weaker, but they were also significantly smaller. Children with CP displayed approximately 70–75% MV of their TD peers, whereas their aCSA was reduced to as little as 55% of their TD peers. This data is consistent with previous reports of diminished muscle size in children using ultrasound [32,35] and MRI [7,16,17]. However, no previous reports have matched the size of children’s muscles with their strength capacity, to document the size–strength relationship in children with CP. We have asked the question: could the reduction in torque production be related to muscle size? In TD children, both morphological measures of MV and aCSA demonstrate strong significant relationships to all variables of strength; this is consistent with the adult and adolescent literature [21]. Furthermore, these correlations (established via MRI) are higher than those reported previously in children using ultrasonography [36]. A strong relationship between muscle size and strength was not evident for children with CP, supporting the third hypothesis. MV demonstrated a weaker correlation to torque
Does muscle size matter?
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in children with CP; however, no correlation could be established between aCSA and any measure of strength in this population. Moreover, Fisher’s Z scores revealed there was a significant difference in the aCSA size–strength relationships between the groups, children with CP consistently demonstrated poorer aCSA size–strength relationships. It is conceivable that MV is a better indicator of growth and development; therefore, a better predictor of the ‘‘strength health’’ of a muscle. As MV is the product of physiological CSA and fiber length, and joint torque is directly affected by both force and length [37], it is likely to be particularly useful in understanding the size–strength relationship in pediatric populations. It is therefore recommended that measurements of muscle morphology in children should include estimates of volume to best represent the capacity of the muscle, particularly when measures of the physiological CSA are unattainable. It is generally accepted that a muscle demonstrates increased force generating capacity during isometric contractions than during concentric contractions [38]. This principle was demonstrated by the TD children, as the greatest size–strength relationship existed between measures of morphology (MV and aCSA) and isometric PT/Bm. However, the strength profiles of children with CP did not follow this principle, demonstrating weak to moderate correlations between MV and isometric PT/Bm. These observations suggest that the muscles of children with CP are not only under-sized but under-powered with respect to producing isometric torque, relative to their muscle size. Although in the present study we did not assess motor unit activation, it appears that deficiencies in neuromotor functioning may partly explain the significant reduction in isometric torque output relative to muscle size; however, they do not appear to be the sole explanation. Whilst children with CP did not conform to the size–strength principle isometrically, they did demonstrate a very interesting size–strength relationship in terms of joint work output. The strongest size–strength relationship existed between MV and joint work output for children with CP. Joint work (j/Bm) is the ability of a muscle(s), via a joint, to produce torque throughout range of motion, and represents the mechanical integrity of the muscle to operate dynamically. These results have demonstrated that children with CP have a significantly diminished capacity to produce work with respect to their TD peers. Such a decrement in a muscles’ capacity to do work may be detrimental to functional performance. However, joint work appears to be the best predictor of muscle morphology in CP, with Pearson’s r values equivalent to the TD population. Therefore, unlike isometric Pt/Bm, the assessment of joint work relative to MV does not appear to be influenced by alterations in neural drive, and may be a better indicator of muscle performance. Increased research attention should be paid to joint work capacity as a potential indicator of muscle health of children with CP.
Conclusions Children with CP have smaller, weaker muscles than their TD peers. However, the size of muscle does not necessarily relate to muscle strength outputs in children with CP. MV appears to be a better predictor of muscle strength than aCSA, and the greatest size–strength relationship exists between MV and joint work output. The weak correlation between MV and isometric PT/Bm suggests children with CP are under-powered relative to their muscle size. Further research is required to elucidate the nature of the size–strength imbalance. Altered neural drive appears to disturb the aCSA size–strength relationship. However, reduced capacity to do work at the joint appears to be more directly related to alterations in muscle volume. This area of research is likely to improve the efficacy of the assessment of muscle strength and
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morphology, and in turn improve treatments that target muscle functioning in children with CP.
Acknowledgements The authors would like to thank Professor Eve Blair for her assistance with the formulation of this manuscript, the Department of Paediatric Rehabilitation, Princess Margaret Hospital (PMH) for their support and assistance with recruitment and the Department of Diagnostic Imaging, PMH, in particular, Alex Kuenzel, for their assistance in data collection. Authors would also like to acknowledge the contribution of the School of Sport Science, Exercise & Health at UWA for the use of equipment and facilities.
Declaration of interest The authors report no conflicts responsible for the content and This project was supported Fellowship and the University and Development Awards.
of interest. The authors alone are writing of this article. by The Raine Medical Research of Western Australia’s Research
References 1. Reddihough DS, Collins KJ. The epidemiology and causes of cerebral palsy. Aust J Physiother 2003;49:7–12. 2. MacPhail H, Kramer J. Effect of isokinetic strength training on functional ability and walking efficiency in adolescents with cerebral palsy. Dev Med Child Neurol 1995;37:763–75. 3. Mayston MJ. People with cerebral palsy: effects of and perspectives for therapy. Neural Plasticity 2001;8:51–69. 4. Dodd KJ, Taylor NF, Damiano DL. A systematic review of the effectiveness of strength-training programs for people with cerebral palsy. Arch Phys Med Rehabil 2002;83:1157–64. 5. Wiley ME, Damiano DL. Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol 1998;40:100–7. 6. Damiano DL, Vaughan CL, Abel MF. Muscle response to heavy resistance exercise in children with spastic cerebral palsy. Dev Med Child Neurol 1995;37:731–9. 7. Elder GCB, Kirk J, Stewart G, et al. Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol 2003;45:542–50. 8. Stackhouse SK, Binder-Macleod SA, Lee SCK. Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 2005;31:594–601. 9. Reid S, Hamer P, Alderson J, Lloyd D. Neuromuscular adaptations to eccentric strength training for adolescents. Dev Med Child Neurol 2010;52:358–63. 10. Damiano D, Arnold A, Steele K, Delp S. Can strength training predictably improve gait kinematics? A pilot study on the effects of hip and knee extensor strengthening on lower extremity alignment in children with cerebral palsy. Phys Ther 2010;90:269–79. 11. Ross SA, Engsberg JR. Relation between spasticity and strength in individuals with spastic diplegic cerebral palsy. Development Med Child Neurol 2002;44:148–57. 12. Rose J, McGill KC. The motor unit in cerebral palsy. Dev Med Child Neurol 1998;40:270–7. 13. Brown JK, Rodda J, Walsh EG, Wright GW. Neurophysiology of lower-limb function in hemiplegic children. Dev Med Child Neurol 1991;33:1037–47. 14. Booth CM, Cortina-Borja MJF, Theologis TN. Collagen accumulation in muscle of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol 2001;43:314–20. 15. Lieber RL, Steinman S, Barash IA, Chambers H. Structural and functional changes in spastic skeletal muscle. Muscle Nerve 2004; 29:615–27. 16. Noble JJ, Fry N, Lewis A, et al. Lower limb muscle volumes in bilateral cerebral palsy. Brain Develop 2014;34:294–300. 17. Shortland A. Muscle deficits in cerebral palsy and early loss of mobility: can we learn something from our elders? Dev Med Child Neurol 2009;51:59–63. 18. Lieber RL, Fride´n J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 2000;23:1647–66.
Disabil Rehabil Downloaded from informahealthcare.com by University of Otago on 01/11/15 For personal use only.
6
S. L. Reid et al.
19. Bamman M, Newcomer B, Larson-Meyer D, et al. Evaluation of the strength-size relationship in vivo using various muscle size indices. Med Sci Sport Exer 2000;32:1307–13. 20. Akagi R, Takai Y, Ohia M, Kanehisa H. Muscle volume compared to cross-sectional area is more appropriate for evaluating muscle strength in young and elderly individuals. Age Ageing 2009;38:1–6. 21. Deighan M, De Ste Croix M, Armstrong N. Measurement of maximal muscle cross-sectional area of knee and elbow extensors and flexors in children, teenagers and adults. J Sports Sci 2006;24: 543–6. 22. Wood LE, Dixon S, Grant C, Armstrong N. Elbow flexion and extension strength relative to body size or muscle size in children. Med Sci Sport Exer 2004;36:1977–84. 23. Voronov A. Anatomical cross-sectional areas and volumes of the muscles of the lower extremities. Human Physiol 2003;29: 201–11. 24. Engstrom C, Loeb G, Reid J, et al. Morphometry of the human thigh muscles. A comparison between anatomical sections and computer tomographic and magnetic resonance images. J Anatomy 1990;176: 139–56. 25. Roy R, Edgerton VIKP. Skeletal muscle architecture and performance. In Komi P, ed. Strength and power in sport. Cambridge: Blackwell Scientific; 1992:115–29. 26. Beunen G, Thomis M. Muscular strength development in children and adolescents. Pediatr Exer Sci 2000;12:174–97. 27. Drouin J, Valovich M. Reliability and validity of the Biodex system 3 pro isokinetic dynamometer velocity, torque and position measurements. J Appl Physiol 2004;91:22–9. 28. De Ste Croix M, Deighan M, Armstrong A. Assessment and interpretation of isokinetic muscle strength during growth and maturation. Sports Med 2003;33:727–43.
Disabil Rehabil, Early Online: 1–6
29. Deighan M, De Ste Croix M, Armstrong N. Reliability of isokinetic knee and elbow strength in 9/10 year old boys. Isokinet Exer Sci 2003;11:209–15. 30. Ayalon M, Ben-Sira D, Hutzler Y, Gilad T. Reliabilty of isokinetic strength measuerment of the knee in children with cerebral palsy. Dev Med Child Neurol 2000;42:398–402. 31. Pitcher C, Elliott C, Williams S, et al. Childhood muscle morphology and strength: alterations over six months of growth. Muscle Nerve 2012;46:360–6. 32. Moreau NG, Teefey SA, Damiano DL. In vivo muscle architecture and size of the rectus femoris and vastus lateralis in children and adolescents with cerebral palsy. Dev Med Child Neurol 2009;51: 800–6. 33. Palisano R, Rosenbaum P, Walter S, et al. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997;39:214–23. 34. Reid S, Hamer P, Alderson J, Lloyd D. Neuromuscular adaptations to eccentric strength training in children and adolescents with cererbal palsy. Dev Med Child Neurol 2010;52:358–63. 35. McNee AE, Gough M, Morrissey MC, Shortland AP. Increases in muscle volume after plantarflexor strength training in children with spastic cerebral palsy. Dev Med Child Neurol 2009; 51:429–35. 36. Kanehisa H, Yata H, Ikegawa S, Fukunaga T. A cross-sectional study of the size and strength of the lower leg muscles during growth. Eur J Appl Physiol 1995;72:150–6. 37. Fukunaga T, Kubo K, Kawakami Y, et al. In vivo behaviour of human muscle tendon during walking. Proc Royal Soc Lond 2001; 268:229–33. 38. Enoka RM. Neuromechanics of human movement. 3rd ed. Champaign (IL): Human Kinetics; 2002.
