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The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy
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Journal of Electromyography and Kinesiology 17 (2007) 657–663 www.elsevier.com/locate/jelekin
The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy Ritu Malaiya, Anne E. McNee, Nicola R. Fry, Linda C. Eve, Martin Gough, Adam P. Shortland * One Small Step Gait Laboratory, Guy’s Hospital, London SE1 9RT, UK
Abstract We collected 3D ultrasound images of the medial gastrocnemius muscle belly (MG) in 16 children with spastic hemiplegic cerebral palsy (SHCP) (mean age: 7.8 years; range: 4–12) and 15 typically-developing (TD) children (mean age: 9.5 years; range: 4–13). All children with SHCP had limited passive dorsiflexion range on the affected side with the knee extended (mean ± 1SD: 9.3° ± 11.8). Scans were taken of both legs with the ankle joint at its resting angle (RA) and at maximum passive dorsiflexion (MD), with the knee extended. RA and MD were more plantar flexed (p < 0.05) in children with SHCP than in TD children. We measured the volumes and lengths of the MG bellies. We also measured the length of muscle fascicles in the mid-portion of the muscle belly and the angle that the fascicles made with the deep aponeurosis of the muscle. Volumes were normalised to the subject’s body mass; muscle lengths and fascicle lengths were normalised to the length of the fibula. Normalised MG belly lengths in the paretic limb were shorter than the non-paretic side at MD (p = 0.0001) and RA (p = 0.0236). Normalised muscle lengths of the paretic limb were shorter than those in TD children at both angles (p = 0.0004; p = 0.0003). However, normalised fascicle lengths in the non-paretic and paretic limbs were similar to those measured in TD children (p > 0.05). When compared to the non-paretic limb, muscle volume was reduced in the paretic limb (p < 0.0001), by an average of 28%, and normalised muscle volume in the paretic limb was smaller than in the TD group (p < 0.0001). The MG is short and small in the paretic limb of children with SHCP. The altered morphology is not due to a decrease in fascicle length. We suggest that MG deformity in SHCP is caused by lack of cross-sectional growth. Ó 2007 Published by Elsevier Ltd. Keywords: Muscle morphology; 3D ultrasound; Spastic hemiplegic cerebral palsy
1. Introduction Spastic cerebral palsy (SCP) is a disorder that arises from a non-progressive lesion of the developing brain. Different types of the condition occur according to the location and pathology of the lesion. The two most common are spastic hemiplegic (SHCP) and diplegic (SDCP) cerebral palsy. Children with these conditions have poor selec-
*
Corresponding author. E-mail address: [email protected] (A.P. Shortland).
1050-6411/$ - see front matter Ó 2007 Published by Elsevier Ltd. doi:10.1016/j.jelekin.2007.02.009
tive control and weakness of some of the musculature in their affected limbs (Engsberg et al., 2000; Wiley and Damiano, 1998; Stackhouse et al., 2005). They reach their motor milestones of sitting and walking later than their typicallydeveloping (TD) peers (Uvebrant, 1988; Fedrizzi et al., 2000). As they mature, they develop shortness of the musculotendinous units (fixed deformities) that contribute to a progressive decline in mobility (Bottos et al., 2001). A more detailed understanding of the nature of deformities may help us to devise new strategies to treat or prevent them. Recently, a number of imaging and physiological studies in children and young adults have elucidated the structure
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of musculature in affected limbs in spastic cerebral palsy. Using MRI, Elder et al. (2003) demonstrated that the calf musculature of the paretic limbs of children with SHCP was on average 73% of the volume of the non-paretic limb. In a group of young adults with SHCP, Lampe et al. (2006) were able to show that all the muscles in the affected lower limb were smaller than in the unaffected limb. They noted that the relative difference in volume was more pronounced for the muscles of the leg than the thigh. However, these authors did not report the architectural origin of the muscle belly deformity, nor did they compare the results to a typically-developing group. Until recently, much of the understanding of muscle deformity has been based on the extrapolation of animal models of immobilisation and tenotomy with the suggestion that muscle fibre shortness was responsible for fixed shortness of the muscle belly (for review see O’Dwyer et al., 1989). However, Heslinga and Huijing (1992) showed that pennate muscles can become short after immobilisation by an alternative mechanism in which the aponeurosis becomes shorter and the muscle loses its force-generating capacity by cross-sectional atrophy. Using 2D ultrasound imaging, we have shown that muscle fibres in the medial gastrocnemius (MG) of children with SDCP are similar in length to those in typically-developing children (Shortland et al., 2002) but the length of the muscle belly of the MG is shorter in the affected group (Fry et al., 2004). Our findings are consistent with cross-sectional atrophy of the fibres, and not fibre shortening, as an explanation of fixed muscle shortness in SDCP. These finding are supported by the work of Lieber and Friden (2002) in the affected upper limbs of children with hemiplegia with wrist flexion contractures. Using a laser diffraction technique, these workers measured much longer sarcomeres in the affected flexor carpi ulnaris (FCU) than in control muscle. In three subjects with spasticity, the slope of the relationship between sarcomere length and wrist joint angle was shown to be similar to the controls. The authors concluded serial sarcomere number and muscle fibre length were essentially normal. Work from Smeulders et al. (2004) contradicts some of these findings. After clinical dissection, Smeulders and his co-workers measured the active and passive force length relationships of FCU in subjects with wrist flexion deformities secondary to spasticity (see also Smeulders and Kreulen, 2007). They found that these muscles operated at optimal active force at positions close to maximum wrist extension. At these lengths, the passive contribution of the FCU to the total force was very small. It should be stated that both these studies were conducted on the FCU prior to surgery to correct wrist flexion deformity. No similar studies have been conducted in the lower limbs of children with SCP. In this study we investigate the gross muscle structure of the MG in vivo in children with SHCP, using a 3D ultrasound imaging technique. 2D ultrasound has been used to measure muscle fascicle lengths in healthy and affected subjects (Narici et al., 1996; Shortland et al., 2002). Ultra-
sound allows the capture of reliable and accurate volumetric data from muscle as shown by Reeves et al. (2004)). While muscle deformities are a feature of both SHCP and SDCP, it is possible that the adaptation of muscle under the two conditions is different. The locations of the cerebral injuries in the two groups are distinct. The distribution of the gestation periods is different in the two groups, and children with SHCP tend to develop their motor milestones earlier than children with SDCP (Uvebrant, 1988). However, on the basis of the data we have collected for subjects with SDCP, we would hypothesise that fascicle lengths of the MG in the affected limb of subjects with SHCP, when normalised to the length of the adjacent bone, are similar to those in the unaffected limb and the limbs of unimpaired subjects. We would also suggest that the affected muscles are smaller and shorter, and that the length and volume of these muscles (normalised to bony length and body mass, respectively) are related. Finally, we should be able to demonstrate that muscle shortness explains the limited passive ankle dorsiflexion range in the affected limb of children with SHCP. 2. Methods This study was approved by the local Research Ethics Committee, and written consent was obtained in all cases from the parent/guardian. Sixteen children with SHCP aged between 4 and 12 years (mean: 7.8 years; 4 male) were recruited from those attending for gait analysis or for clinical review at a tertiary centre. All children had limited passive dorsiflexion range, had no previous surgical intervention and had not received Botulinum toxin in the 6 months prior to scanning. Fifteen TD subjects were recruited from the children of friends and colleagues of the investigators (4– 13 years; mean: 9.5 years; 6 male). Some anthropometric and other data for these children are given in Table 1. A freehand magnetic 3D tracking system (CompactScan, TomTec Gmbh, Germany) was used to acquire the images from the video output of an ultrasound scanner (SSD-1000, ALOKA, Japan) while simultaneously recording position and orientation of the ultrasonic probe. By interpolation of the semi-structured array of images, 3D representations of the scanned anatomical feature may be reconstructed. Scanning took place with the subjects prone with their knees extended and their ankles overhanging the edge of the plinth. All measurements were made on a wooden couch to reduce the development of eddy currents due to the magnetic field generated by the 3D tracking system, providing volumetric reconstructions without significant distortions. A 7.5MHz linear array probe with an effective scanning width of 6 cm was found to be sufficient to acquire the maximum width of the medial gastrocnemius within the field of view. Longitudinal scans were taken from the calcaneum to the femoral condyles following the courses of the Achilles tendon and the medial head of the gastrocnemius. Scans were taken on both legs at the resting ankle angle (relaxed position of the foot with no external force applied by the examiner, i.e. gravity and internal forces determining the position) and at the angle of maximum passive dorsiflexion (achieved through manual manipulation) with the knee in extension. These ankle positions were measured using a plastic goniometer. Par-
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Table 1 Details of the children recruited to the study indicated as mean ± 1SD
Age (years) Body mass (kg) Height (m) Lower limb length (m) Fibular length (m) Maximum dorsiflexion (°) (knee extended) Resting ankle angle (°) (knee extended) a b
Typically developing
SHCP (non-paretic)
SHCP (paretic)
9.5 (4–13) 32.12 ± 10.77 1.351 ± 0.075 0.698 ± 0.106 0.287 ± 0.043 14.1 ± 8.3a 18.0 ± 6.0a
7.8 (4–12) 26.87 ± 10.79 1.246 ± 0.132 0.637 ± 0.081b 0.267 ± 0.039b 11.8 ± 6.7b 20.4 ± 7.1b
N/A N/A N/A 0.628 ± 0.078 0.261 ± 0.041 9.3 ± 11.8 34.4 ± 10.7
Indicates a significant difference between the typically-developing children and the affected limbs of children with SHCP. Indicates a significant difference between unaffected and affected limbs in the SHCP group.
ticipants were encouraged to relax and not to aid or resist passive movement of the ankle. The reconstructed volumes were stored in a proprietary digital format on the CompactScan. Sagittal, coronal and transverse sections through the reconstructed volume could be viewed simultaneously and rotated around a fixed point to obtain the best view of the muscle structures using the supplied software (TomTec EchoScan 4.2). Muscle belly length was estimated by measuring the linear distance between the most superficial tip of the medial femoral condyle and the most distal end of the muscle belly. The distal point within the belly was identified by inspecting the 3D volume in transverse, longitudinal and oblique planes. Muscle belly length was normalised to fibular length. Muscle fascicle length was measured as the linear distance between the insertion of a fascicle into the lower and upper aponeurosis. Measurements were made at a point half way along the length of the muscle and at about half the width of the muscle. The angle between this fascicle and the deep aponeurosis (the deep fascicular-aponeurosis angle) was also measured. These data were normalised to fibular length. Muscle cross-sectional area was measured at each of twelve equally-spaced sections along the length of the muscle. Volume was calculated using disk summation. Volume data was normalised to body mass. Data from paretic or non-paretic limbs and TD limbs were compared using unpaired student’s t-tests (p < 0.05). Data between affected and unaffected limbs were compared using paired t-tests (p < 0.05). The strength of relationships between
variables was determined by computing the adjusted coefficient of determination ðR2adj Þ from simple linear regression analysis.
3. Results The mean age, weight, height, and lower limb and fibular length of the group of TD children were greater than those of the children with SHCP, but none of these differences reached statistical significance (Table 1). The affected limb of the children with SHCP was on average about 1 cm shorter than the unaffected limb (p < 0.05), as was the fibular length. The limbs of TD children and the non-paretic limbs of children with SHCP had greater passive ankle dorsiflexion range and a much less plantar flexed resting ankle angle than the affected limb (p < 0.05). We found that the MG in the paretic limb was about two-thirds of the volume of the muscle in the non-paretic or TD limbs, when normalised to body mass (p < 0.05) (Table 2). The muscle in the affected limb was on average 10% shorter than in the limbs of TD children, and a little shorter than in the unaffected limb (p < 0.05). At the resting ankle angle, the MG belly of the non-paretic limb was shorter than the TD MG (p < 0.05) but the muscle was of similar volume. Fascicle lengths had similar mean values at rest and at maximum passive dorsiflexion for all the limbs investigated. However, we found the deep fascicle
Table 2 Details of the morphological and architectural data in the MG of typically developing children and the children with SHCP indicated as mean ± 1SD Muscle volume (cm3) Normalised muscle volume (cm3/kg) Muscle length (m) (maximum dorsiflexion) Muscle length (m) (resting ankle position) Normalised muscle length (maximum dorsiflexion) Normalised muscle length (resting ankle position) Fascicle length (m) (maximum dorsiflexion) Fascicle length (m) (resting ankle position) Normalised fascicle length (maximum dorsiflexion) Normalised fascicle length (resting ankle position) DFA angle (°) (maximum dorsiflexion) DFA angle (°) (resting ankle angle) a b c
Typically developing
SHCP (non-paretic)
SHCP (paretic)
82.1 ± 27.3a 2.60 ± 0.46a 0.204 ± 0.033a, b 0.191+/0.035a,b 0.71 ± 0.04a 0.67 ± 0.05a,b 0.049 ± 0.004 0.045 ± 0.007a 0.175 ± 0.022 0.157 ± 0.020 15.8 ± 1.2a,b 17.0 ± 1.9
66.4 ± 16.9c 2.47 ± 0.65c 0.181 ± 0.028c 0.165 ± 0.028c 0.68 ± 0.06c 0.62 ± 0.06c 0.050 ± 0.010 0.041 ± 0.006 0.19 ± 0.03 0.16 ± 0.03 13.13 ± 3.75 16.22 ± 3.55
48.1 ± 16.8 1.69 ± 0.48 0.166 ± 0.026 0.157 ± 0.025 0.63 ± 0.06 0.60 ± 0.05 0.045 ± 0.008 0.038 ± 0.0081 0.18 ± 0.04 0.15 ± 0.03 14.11 ± 2.64 15.91 ± 3.47
Indicates a significant difference between the typically-developing children and the affected limbs of children with SHCP. Indicates a significant difference between typically-developing children and the unaffected limbs of the children with SHCP. Indicates a significant difference between unaffected and affected limbs in the SHCP group.
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aponeurosis angle (DFA) to be shallower in both limbs of the children with SHCP than in their TD peers, by about 2° on average. The tabulated results suggest that the lack of longitudinal growth in the affected MG is not a function of reduced fascicle length. We wished to investigate if the length of the affected muscle belly was related to the lack of volumetric growth that we have noted. We found a significant linear relationship between normalised muscle length and the normalised muscle volume to the power of 2/3 (R2adj ¼ 0:403, p = 0.007) in the SHCP group, while we found no such relationship for the data from TD subjects (R2adj ¼ 0:07, p = 0.33) (Fig. 1). The relationship between morphological and clinical measures of deformity should be of particular interest to the clinical community. We found no significant linear relationship between muscle belly length and ankle joint angle at maximum passive dorsiflexion or at the resting ankle angle (max. passive dors: R2adj ¼ 0:057, p = 0.673; resting ankle angle: R2adj ¼ 0:041, p = 0.22) (Fig. 2).
Normalised Muscle Length
0.75
0.7
0.65
0.6
0.55
0.5 0
0.5
1
1.5
2
2.5
2/3
Normalised Muscle Volume
Fig. 1. The relationship between normalised MG volume raised to the power of 2/3 and normalised MG length for the affected limb of children with SHCP (filled circles) and for TD children (open squares).
Normalised MG length
0.9 0.8 0.7 0.6 0.5 0.4 0.3 -60
-50
-40
-30
-20
-10
0
10
20
Ankle Angle (o) Fig. 2. The relationships between normalised muscle length and ankle angle at maximum passive dorsiflexion (open diamonds) and at the resting ankle angle (closed triangles).
4. Discussion We measured the MG volume, belly length, fascicle length and DFA in the affected and unaffected limbs of children with SHCP, and in a group of TD children. The affected limbs of children with SHCP demonstrated limited passive dorsiflexion range and greatly plantar flexed resting ankle angles. Our expectation that the MG of paretic limbs in SHCP would be shorter and smaller than in non-paretic and TD limbs was met, and our hypothesis that the shortness of the MG could not be explained by a reduction in fascicular length was proven. Normalised fascicle lengths in the paretic limbs were not significantly different to those in the limbs of TD subjects or in the non-paretic limb and the mean values were similar. Importantly, there was a significant relationship between normalised MG volume and normalised MG length in the affected limb of SHCP indicating that the fixed shortness of the MG belly is related to the failure of volumetric muscle growth. Intriguingly, muscle length in the affected limb, as measured by 3D ultrasound, was not related to the passive ankle dorsiflexion range or resting ankle angle. It is difficult to reconcile some of the differences we observed in the architecture and morphology of the MG in the non-paretic limb to TD muscle. Normalised MG volumes in the non-paretic limb were similar to those of the TD subjects but the muscles were significantly shorter at the resting angle. This could not be explained by a reduction in fascicular length and/or an increase in DFA as might be expected if we consider the MG to have parallelogram planar symmetry. It is possible that there are subtle differences in the 3D shape of the muscle that allows an altered distribution of fascicle lengths and angles for a given muscle length. While the small differences between non-paretic and typically-developing muscle are of interest they are unlikely to be of clinical importance. 4.1. Limitations of the study This paper relies on the assumption that the resting ankle angle with the knee extended equates approximately to the resting length of the muscle (gastrocnemius). In fact, a small tensile force will be exerted on the plantar flexors by the mass of the foot acting around the pivot of the ankle. The assumption may veer further from the truth if one of the other triceps surae is more involved than the MG, making the ankle more plantar flexed than by the MG alone. For additional discussions on this point see Yucesoy and Huijing (2007) and Huijing (2007). In addition, significant muscle activity in the plantar flexor or pretibial muscle groups could alter the resting angle during measurement. Although, we encouraged all the subjects to relax, we cannot guarantee the muscles of the calf were electrically silent. If either of these error conditions were significant, then the results concerning belly length at this resting ankle angle may carry less importance. This work may be criticised for not including a measurement of morphology at a refer-
Table 3 A fragment of the results (table from Shortland et al., 2002) Ankle joint angle (°) 30 Fascicle length (mm) Typically developing children Children with SDCP Normalised fascicle length Typically developing children Children with SDCP
Resting ankle position
36.1 ± 6.3 38.3 ± 11.5
37.4 ± 10.1 31.8 ± 9.8
0.126 ± 0.022 0.148 ± 0.042
0.130 ± 0.036 0.118 ± 0.031
The original and normalised results for fascicle length at a common angle, and at the resting ankle angle, are illustrated.
a
140 120
661
100 80 60 40 20 0 0
10
20
30
40
50
60
Body Mass (kg)
Muscle Length (mm)
b
300 250 200 150 100 50 150
200
250
300
350
400
350
400
Fibular length (mm)
c
70
Fascicle Length (mm)
ence or common ankle angle. Our reasoning for excluding these measures follows. The children with SHCP studied here represent a group with diverse resting ankle angles and angles of maximum passive dorsiflexion. A common ankle angle to both TD and SHCP groups would be in the order of 30° of plantar flexion. This angle would represent mechanically different states in the MG of affected and unaffected limbs: in TD children the MG would be in an unloaded state, while most of the muscles in the affected limbs of children with SHCP would be under stretch (please refer to Table 1). This is illustrated from our historical data collected on subjects with SDCP and with no pathology, using 2D ultrasound (Table 3; Shortland et al., 2002). The length of fascicles in TD children were very similar at the resting angle and a common ankle angle (30° of plantar flexion) while in children with SDCP the fascicle lengths were significantly longer at the common angle. The inclusion of a common angle may be valuable in a study of children with milder deformities. Under these circumstances, a common angle may be found in which the musculature is place under stretch in both affected and TD groups. Our results are limited to describing the morphology of the MG. It is possible that the morphology of different muscles in the paretic limb is altered according to their function and position within the musculoskeletal system. Recently, a study by Lampe et al. (2006) demonstrated that all the principal muscles in the paretic limbs of a group of young adults with SHCP were smaller than in the nonparetic limb. Using MRI, they found that the muscles of the thigh were more voluminous when compared to those in the non-paretic limb than the muscles of the leg (tibial segment). They reported a similar reduction in the volume of the gastrocnemius when compared to the unaffected limb to that reported here. This paper assumes that normalisation of muscle and fascicle length to skeletal length and muscle volume to body mass minimises the non-clinical variation in these parameters. Fig. 3a and b depicts strong relationships between muscle belly length at the resting ankle angle and fibular length (simple linear regression: R2adj ¼ 0:91, p < 0.00001), and muscle volume and body mass (R2adj ¼ 0:67, p = 0.00032), amongst the TD subjects. However, although there was a significant relationship between fascicle length and fibular length (p = 0.015), Simple linear regression analysis demonstrates that only 37% of fascicle length in
Muscle Volume (cm3)
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60 50 40 30 20 10 0 150
200
250
300
Fibular length (mm) Fig. 3. The relationship between resting muscle dimensions and selected anthropometric variables for TD children and (open squares) the affected limb of children with SHCP (closed circles): (a) muscle volume vs. body mass; (b) muscle length vs. fibular length; (c) muscle fascicle length vs. fibular length.
the TD group is explained by fibular length (Fig. 3c). It is possible that other anthropometric variables influence fascicle length in TD populations including the magnitude of the moment arms that the MG crosses. These relationships could be delineated with larger numbers of subjects and a suitable method for measuring a number of anthropometric variables including moment arms (Maganaris et al., 2006). As for TD muscle, much of the variation in volume and length of the MG in the paretic limb is explained by body mass (R2adj ¼ 0:63, p = 0.00025) and fibular length (R2adj ¼ 0:62, p = 0.00046), respectively (Fig. 3a and b). However, we could find no significant relationship between fascicular length and fibular length in the MG of the affected limb (p > 0.05) (Fig. 3c).
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4.2. Clinical implications Our main results have implications for understanding the relationship between muscle deformity and function in children with SHCP. A number of workers have measured the voluntary strength of the calf muscles in children with SCP (Elder et al., 2003; Stackhouse et al., 2005). The deficits in force production reported were attributed, in part, to the reduced voluntary activation of this muscle group, and to the coactivation with antagonist muscle groups. Our findings suggest that a large proportion of the weakness of the calf musculature is caused by a mechanical deficit related to a significant reduction in volume. It is likely that deleterious changes to muscle fibres and the proliferation of the extracellular matrix also contribute to the poor mechanical function of muscle in this group (Booth et al., 2001; Lieber et al., 2003). Our results indicate that the failure of growth of the affected muscle was not caused by short fascicles but by a reduction in cross-section (Fig. 1). The origins of these differences at the cellular level are unclear but it is possible that a reduction in muscle fibre diameter (Lieber et al., 2003) and/or a reduction in the number of fibres (through premature cell death) is responsible. The relationship between the passive range at a joint and the dimensions of the muscle bellies crossing that joint has not been studied to our knowledge. The children with SHCP in this study presented with a wide range of limitations in maximum passive ankle dorsiflexion and a wide range of muscle volumes and lengths. Importantly, we did not find a relationship between normalised muscle length and ankle angle at the resting angle or maximum dorsiflexion (Fig. 2). This study included a limited number of ambulant children and measurements were made on a single muscle so care needs to exercised in extrapolating our results to the other muscles in the lower limb. However, if the poor relationships between joint range and muscle dimensions are confirmed for other muscles and joints then we may have to consider musculotendinous shortness (limited passive range) and muscle belly deformity (reduced muscle volume) as distinct phenomena in the child with SHCP. Acknowledgements Nicola Fry was supported by an Award from the National Co-ordinating Centre for Research Capacity Development (UK). Anne McNee was supported by award from Sports Aiding Medical Research in Kids (SPARKS). References Booth CM, Cortina-Borja MJ, Theologis TN. Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol 2001;43(5):314–20. Bottos M, Feliciangeli A, Sciuto L, Gericke C, Vianello A. Functional status of adults with cerebral palsy and implications for treatment of children. Dev Med Child Neurol 2001;43(8):516–28. Elder GC, Kirk J, Stewart G, Cook K, Weir D, Marshall A, et al.. Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol 2003;45(8):542–50.
Engsberg JR, Ross SA, Olree KS, Park TS. Ankle spasticity and strength in children with spastic diplegic cerebral palsy. Dev Med Child Neurol 2000;42(1):42–7. Fedrizzi E, Facchin P, Marzaroli M, Pagliano E, Botteon G, Percivalle L, et al.. Predictors of independent walking in children with spastic diplegia. J Child Neurol 2000;15(4):228–34. Fry NR, Gough M, Shortland AP. 3D realisation of muscle morphology and architecture using ultrasound. Gait Posture 2004;20(2):177–82. Heslinga JW, Huijing PA. Effects of short length immobilization of medial gastrocnemius muscle of growing young adult rats. Eur J Morphol 1992;30(4):257–73. Huijing PA. Epimuscular myofascial force transmission between antagonistic and synergistic muscles can explain movement limitation in spastic paresis. J Electromyogr Kinesiol 2007;17:708–24. doi:10.1016/ j.jelekin.2007.02.003. Lampe R, Grassl S, Mitternacht J, Gerdesmeyer L, Gradinger R. MRTmeasurements of muscle volumes of the lower extremities of youths with spastic hemiplegia caused by cerebral palsy. Brain Dev 2006;28(8):500–6. Lieber RL, Friden J. Spasticity causes a fundamental rearrangement of muscle–joint interaction. Muscle Nerve 2002;25(2):265–70. Lieber RL, Runesson E, Einarsson F, Friden J. Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material. Muscle Nerve 2003;28(4):464–71. Maganaris CN, Baltzopoulos V, Tsaopoulos D. Muscle fibre length-tomoment arm ratios in the human lower limb determined in vivo. J Biomech 2006;39(9):1663–8. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli P. In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J Physiol 1996;496(Pt 1):287–97. O’Dwyer NJ, Neilson PD, Nash J. Mechanisms of muscle growth related to muscle contracture in cerebral palsy. Dev Med Child Neurol 1989;31:543–52. Reeves ND, Maganaris CN, Narici MV. Ultrasonographic assessment of human skeletal muscle size. Eur J Appl Physiol 2004;91(1):116–8. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the medial gastrocnemius in children with spastic diplegia. Dev Med Child Neurol 2002;44:158–63. Smeulders MJC, Kreulen M, Joris Hage J, Huijing PA, van der Horst CMAM. Overstretching of sarcomeres may not cause cerebral palsy muscle contracture. J Orthop Res 2004;22(6):1331–5. Smeulders MJC, Kreulen M. Myofascial force transmission and tendon transfer for patients suffering from spastic paresis: a review and some new observations. J Electromyogr Kinesiol 2007;17:644–56. doi:10.1016/j.jelekin.2007.02.002. Stackhouse SK, Binder-Macleod SA, Lee SC. Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 2005;31(5):594–601. Uvebrant P. Hemiplegic cerebral palsy. Aetiology and outcome. Acta Paediatr Scand Suppl 1988;345:1–100. Wiley ME, Damiano DL. Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol 1998;40(2):100–7. Yucesoy CA, Huijing PA. Substantial effects of epimuscular myofascial force transmission on muscular mechanics have major implications on spastic muscle and remedial surgery. J Electromyogr Kinesiol 2007;17:664–79. doi:10.1016/j.jelekin.2007.02.008. Dr. Ritu Malaiya is a house officer at Kingston Hospital, London. Her clinical interests include rheumatology and radiology. The work in this paper was carried out as a part of her intercalated Bachelor of Science degree during her medical studies at Guy’s, King’s & St. Thomas’ Medical School, London, UK.
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Anne McNee MPhty is a Research Physiotherapist in the Paediatric Neurosciences Unit in Guy’s & St. Thomas’ Foundation Hospital Trust. Anne is interested in the effect of immobilisation therapy, botulinum toxin and strengthening on the morphology of muscles. She is currently conducting a population study on the relationship between deformity, function and quality of life in older children and young adults with bilateral cerebral palsy.
Dr. M Gough MCh FRCS(Orth), Consultant Paediatric Orthopaedic Surgeon, Guy’s and St. Thomas NHS Foundation Trust, London. He has a special interest in the orthopaedic management of children with neuromuscular deformity, and research interests in the natural history of deformity, its effect on function, and the effect of intervention.
Nicola Fry MSc, Research Clinical Scientist at One Small Step Gait Laboratory, Guy’s & St. Thomas’ NHS Foundation Trust, London. Nicola has developed a 3D ultrasound technique for measuring the volume of muscles and has undertaken research projects which utilise this technique. She is currently working towards her PhD looking at musculo-skeletal deformity in cerebral palsy.
Adam Shortland PhD, Consultant Clinical Scientist and Gait Analysis Service Manager at Guy’s & St. Thomas NHS Foundation Trust and Honorary Senior Lecturer, King’s College, London. His pre-doctoral and postdoctoral studies included ultrasound imaging, biofluid dynamics, muscle mechanics and biomaterials at Sheffield and Liverpool University Medical Schools, UK. He is currently researching the musculoskeletal mechanisms for declining mobility in children with spastic cerebral palsy. Presently, Chairman of the Rehabilitation Engineering and Biomechanics Special Interest Group of the Institute of Physics and Engineering in Medicine (UK).
Linda Eve MCSP, clinical specialist physiotherapist, trained at the London Hospital and specialised in paediatrics with a special interest in cerebral palsy. She worked at the Cheyne Centre for Spastic Children, and was involved with the identification of levels of ability at this centre. She worked in community paediatrics before taking on her current post at the One Small Step Gait Laboratory at Guy’s & St Thomas’ NHS Foundation Trust. Here she has been involved in investigating kinetics in assisted ambulation and has also contributed to setting standards in gait analysis for the clinical laboratories in the UK.
Journal of Electromyography and Kinesiology 17 (2007) 657–663 www.elsevier.com/locate/jelekin
The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy Ritu Malaiya, Anne E. McNee, Nicola R. Fry, Linda C. Eve, Martin Gough, Adam P. Shortland * One Small Step Gait Laboratory, Guy’s Hospital, London SE1 9RT, UK
Abstract We collected 3D ultrasound images of the medial gastrocnemius muscle belly (MG) in 16 children with spastic hemiplegic cerebral palsy (SHCP) (mean age: 7.8 years; range: 4–12) and 15 typically-developing (TD) children (mean age: 9.5 years; range: 4–13). All children with SHCP had limited passive dorsiflexion range on the affected side with the knee extended (mean ± 1SD: 9.3° ± 11.8). Scans were taken of both legs with the ankle joint at its resting angle (RA) and at maximum passive dorsiflexion (MD), with the knee extended. RA and MD were more plantar flexed (p < 0.05) in children with SHCP than in TD children. We measured the volumes and lengths of the MG bellies. We also measured the length of muscle fascicles in the mid-portion of the muscle belly and the angle that the fascicles made with the deep aponeurosis of the muscle. Volumes were normalised to the subject’s body mass; muscle lengths and fascicle lengths were normalised to the length of the fibula. Normalised MG belly lengths in the paretic limb were shorter than the non-paretic side at MD (p = 0.0001) and RA (p = 0.0236). Normalised muscle lengths of the paretic limb were shorter than those in TD children at both angles (p = 0.0004; p = 0.0003). However, normalised fascicle lengths in the non-paretic and paretic limbs were similar to those measured in TD children (p > 0.05). When compared to the non-paretic limb, muscle volume was reduced in the paretic limb (p < 0.0001), by an average of 28%, and normalised muscle volume in the paretic limb was smaller than in the TD group (p < 0.0001). The MG is short and small in the paretic limb of children with SHCP. The altered morphology is not due to a decrease in fascicle length. We suggest that MG deformity in SHCP is caused by lack of cross-sectional growth. Ó 2007 Published by Elsevier Ltd. Keywords: Muscle morphology; 3D ultrasound; Spastic hemiplegic cerebral palsy
1. Introduction Spastic cerebral palsy (SCP) is a disorder that arises from a non-progressive lesion of the developing brain. Different types of the condition occur according to the location and pathology of the lesion. The two most common are spastic hemiplegic (SHCP) and diplegic (SDCP) cerebral palsy. Children with these conditions have poor selec-
*
Corresponding author. E-mail address: [email protected] (A.P. Shortland).
1050-6411/$ - see front matter Ó 2007 Published by Elsevier Ltd. doi:10.1016/j.jelekin.2007.02.009
tive control and weakness of some of the musculature in their affected limbs (Engsberg et al., 2000; Wiley and Damiano, 1998; Stackhouse et al., 2005). They reach their motor milestones of sitting and walking later than their typicallydeveloping (TD) peers (Uvebrant, 1988; Fedrizzi et al., 2000). As they mature, they develop shortness of the musculotendinous units (fixed deformities) that contribute to a progressive decline in mobility (Bottos et al., 2001). A more detailed understanding of the nature of deformities may help us to devise new strategies to treat or prevent them. Recently, a number of imaging and physiological studies in children and young adults have elucidated the structure
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of musculature in affected limbs in spastic cerebral palsy. Using MRI, Elder et al. (2003) demonstrated that the calf musculature of the paretic limbs of children with SHCP was on average 73% of the volume of the non-paretic limb. In a group of young adults with SHCP, Lampe et al. (2006) were able to show that all the muscles in the affected lower limb were smaller than in the unaffected limb. They noted that the relative difference in volume was more pronounced for the muscles of the leg than the thigh. However, these authors did not report the architectural origin of the muscle belly deformity, nor did they compare the results to a typically-developing group. Until recently, much of the understanding of muscle deformity has been based on the extrapolation of animal models of immobilisation and tenotomy with the suggestion that muscle fibre shortness was responsible for fixed shortness of the muscle belly (for review see O’Dwyer et al., 1989). However, Heslinga and Huijing (1992) showed that pennate muscles can become short after immobilisation by an alternative mechanism in which the aponeurosis becomes shorter and the muscle loses its force-generating capacity by cross-sectional atrophy. Using 2D ultrasound imaging, we have shown that muscle fibres in the medial gastrocnemius (MG) of children with SDCP are similar in length to those in typically-developing children (Shortland et al., 2002) but the length of the muscle belly of the MG is shorter in the affected group (Fry et al., 2004). Our findings are consistent with cross-sectional atrophy of the fibres, and not fibre shortening, as an explanation of fixed muscle shortness in SDCP. These finding are supported by the work of Lieber and Friden (2002) in the affected upper limbs of children with hemiplegia with wrist flexion contractures. Using a laser diffraction technique, these workers measured much longer sarcomeres in the affected flexor carpi ulnaris (FCU) than in control muscle. In three subjects with spasticity, the slope of the relationship between sarcomere length and wrist joint angle was shown to be similar to the controls. The authors concluded serial sarcomere number and muscle fibre length were essentially normal. Work from Smeulders et al. (2004) contradicts some of these findings. After clinical dissection, Smeulders and his co-workers measured the active and passive force length relationships of FCU in subjects with wrist flexion deformities secondary to spasticity (see also Smeulders and Kreulen, 2007). They found that these muscles operated at optimal active force at positions close to maximum wrist extension. At these lengths, the passive contribution of the FCU to the total force was very small. It should be stated that both these studies were conducted on the FCU prior to surgery to correct wrist flexion deformity. No similar studies have been conducted in the lower limbs of children with SCP. In this study we investigate the gross muscle structure of the MG in vivo in children with SHCP, using a 3D ultrasound imaging technique. 2D ultrasound has been used to measure muscle fascicle lengths in healthy and affected subjects (Narici et al., 1996; Shortland et al., 2002). Ultra-
sound allows the capture of reliable and accurate volumetric data from muscle as shown by Reeves et al. (2004)). While muscle deformities are a feature of both SHCP and SDCP, it is possible that the adaptation of muscle under the two conditions is different. The locations of the cerebral injuries in the two groups are distinct. The distribution of the gestation periods is different in the two groups, and children with SHCP tend to develop their motor milestones earlier than children with SDCP (Uvebrant, 1988). However, on the basis of the data we have collected for subjects with SDCP, we would hypothesise that fascicle lengths of the MG in the affected limb of subjects with SHCP, when normalised to the length of the adjacent bone, are similar to those in the unaffected limb and the limbs of unimpaired subjects. We would also suggest that the affected muscles are smaller and shorter, and that the length and volume of these muscles (normalised to bony length and body mass, respectively) are related. Finally, we should be able to demonstrate that muscle shortness explains the limited passive ankle dorsiflexion range in the affected limb of children with SHCP. 2. Methods This study was approved by the local Research Ethics Committee, and written consent was obtained in all cases from the parent/guardian. Sixteen children with SHCP aged between 4 and 12 years (mean: 7.8 years; 4 male) were recruited from those attending for gait analysis or for clinical review at a tertiary centre. All children had limited passive dorsiflexion range, had no previous surgical intervention and had not received Botulinum toxin in the 6 months prior to scanning. Fifteen TD subjects were recruited from the children of friends and colleagues of the investigators (4– 13 years; mean: 9.5 years; 6 male). Some anthropometric and other data for these children are given in Table 1. A freehand magnetic 3D tracking system (CompactScan, TomTec Gmbh, Germany) was used to acquire the images from the video output of an ultrasound scanner (SSD-1000, ALOKA, Japan) while simultaneously recording position and orientation of the ultrasonic probe. By interpolation of the semi-structured array of images, 3D representations of the scanned anatomical feature may be reconstructed. Scanning took place with the subjects prone with their knees extended and their ankles overhanging the edge of the plinth. All measurements were made on a wooden couch to reduce the development of eddy currents due to the magnetic field generated by the 3D tracking system, providing volumetric reconstructions without significant distortions. A 7.5MHz linear array probe with an effective scanning width of 6 cm was found to be sufficient to acquire the maximum width of the medial gastrocnemius within the field of view. Longitudinal scans were taken from the calcaneum to the femoral condyles following the courses of the Achilles tendon and the medial head of the gastrocnemius. Scans were taken on both legs at the resting ankle angle (relaxed position of the foot with no external force applied by the examiner, i.e. gravity and internal forces determining the position) and at the angle of maximum passive dorsiflexion (achieved through manual manipulation) with the knee in extension. These ankle positions were measured using a plastic goniometer. Par-
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Table 1 Details of the children recruited to the study indicated as mean ± 1SD
Age (years) Body mass (kg) Height (m) Lower limb length (m) Fibular length (m) Maximum dorsiflexion (°) (knee extended) Resting ankle angle (°) (knee extended) a b
Typically developing
SHCP (non-paretic)
SHCP (paretic)
9.5 (4–13) 32.12 ± 10.77 1.351 ± 0.075 0.698 ± 0.106 0.287 ± 0.043 14.1 ± 8.3a 18.0 ± 6.0a
7.8 (4–12) 26.87 ± 10.79 1.246 ± 0.132 0.637 ± 0.081b 0.267 ± 0.039b 11.8 ± 6.7b 20.4 ± 7.1b
N/A N/A N/A 0.628 ± 0.078 0.261 ± 0.041 9.3 ± 11.8 34.4 ± 10.7
Indicates a significant difference between the typically-developing children and the affected limbs of children with SHCP. Indicates a significant difference between unaffected and affected limbs in the SHCP group.
ticipants were encouraged to relax and not to aid or resist passive movement of the ankle. The reconstructed volumes were stored in a proprietary digital format on the CompactScan. Sagittal, coronal and transverse sections through the reconstructed volume could be viewed simultaneously and rotated around a fixed point to obtain the best view of the muscle structures using the supplied software (TomTec EchoScan 4.2). Muscle belly length was estimated by measuring the linear distance between the most superficial tip of the medial femoral condyle and the most distal end of the muscle belly. The distal point within the belly was identified by inspecting the 3D volume in transverse, longitudinal and oblique planes. Muscle belly length was normalised to fibular length. Muscle fascicle length was measured as the linear distance between the insertion of a fascicle into the lower and upper aponeurosis. Measurements were made at a point half way along the length of the muscle and at about half the width of the muscle. The angle between this fascicle and the deep aponeurosis (the deep fascicular-aponeurosis angle) was also measured. These data were normalised to fibular length. Muscle cross-sectional area was measured at each of twelve equally-spaced sections along the length of the muscle. Volume was calculated using disk summation. Volume data was normalised to body mass. Data from paretic or non-paretic limbs and TD limbs were compared using unpaired student’s t-tests (p < 0.05). Data between affected and unaffected limbs were compared using paired t-tests (p < 0.05). The strength of relationships between
variables was determined by computing the adjusted coefficient of determination ðR2adj Þ from simple linear regression analysis.
3. Results The mean age, weight, height, and lower limb and fibular length of the group of TD children were greater than those of the children with SHCP, but none of these differences reached statistical significance (Table 1). The affected limb of the children with SHCP was on average about 1 cm shorter than the unaffected limb (p < 0.05), as was the fibular length. The limbs of TD children and the non-paretic limbs of children with SHCP had greater passive ankle dorsiflexion range and a much less plantar flexed resting ankle angle than the affected limb (p < 0.05). We found that the MG in the paretic limb was about two-thirds of the volume of the muscle in the non-paretic or TD limbs, when normalised to body mass (p < 0.05) (Table 2). The muscle in the affected limb was on average 10% shorter than in the limbs of TD children, and a little shorter than in the unaffected limb (p < 0.05). At the resting ankle angle, the MG belly of the non-paretic limb was shorter than the TD MG (p < 0.05) but the muscle was of similar volume. Fascicle lengths had similar mean values at rest and at maximum passive dorsiflexion for all the limbs investigated. However, we found the deep fascicle
Table 2 Details of the morphological and architectural data in the MG of typically developing children and the children with SHCP indicated as mean ± 1SD Muscle volume (cm3) Normalised muscle volume (cm3/kg) Muscle length (m) (maximum dorsiflexion) Muscle length (m) (resting ankle position) Normalised muscle length (maximum dorsiflexion) Normalised muscle length (resting ankle position) Fascicle length (m) (maximum dorsiflexion) Fascicle length (m) (resting ankle position) Normalised fascicle length (maximum dorsiflexion) Normalised fascicle length (resting ankle position) DFA angle (°) (maximum dorsiflexion) DFA angle (°) (resting ankle angle) a b c
Typically developing
SHCP (non-paretic)
SHCP (paretic)
82.1 ± 27.3a 2.60 ± 0.46a 0.204 ± 0.033a, b 0.191+/0.035a,b 0.71 ± 0.04a 0.67 ± 0.05a,b 0.049 ± 0.004 0.045 ± 0.007a 0.175 ± 0.022 0.157 ± 0.020 15.8 ± 1.2a,b 17.0 ± 1.9
66.4 ± 16.9c 2.47 ± 0.65c 0.181 ± 0.028c 0.165 ± 0.028c 0.68 ± 0.06c 0.62 ± 0.06c 0.050 ± 0.010 0.041 ± 0.006 0.19 ± 0.03 0.16 ± 0.03 13.13 ± 3.75 16.22 ± 3.55
48.1 ± 16.8 1.69 ± 0.48 0.166 ± 0.026 0.157 ± 0.025 0.63 ± 0.06 0.60 ± 0.05 0.045 ± 0.008 0.038 ± 0.0081 0.18 ± 0.04 0.15 ± 0.03 14.11 ± 2.64 15.91 ± 3.47
Indicates a significant difference between the typically-developing children and the affected limbs of children with SHCP. Indicates a significant difference between typically-developing children and the unaffected limbs of the children with SHCP. Indicates a significant difference between unaffected and affected limbs in the SHCP group.
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aponeurosis angle (DFA) to be shallower in both limbs of the children with SHCP than in their TD peers, by about 2° on average. The tabulated results suggest that the lack of longitudinal growth in the affected MG is not a function of reduced fascicle length. We wished to investigate if the length of the affected muscle belly was related to the lack of volumetric growth that we have noted. We found a significant linear relationship between normalised muscle length and the normalised muscle volume to the power of 2/3 (R2adj ¼ 0:403, p = 0.007) in the SHCP group, while we found no such relationship for the data from TD subjects (R2adj ¼ 0:07, p = 0.33) (Fig. 1). The relationship between morphological and clinical measures of deformity should be of particular interest to the clinical community. We found no significant linear relationship between muscle belly length and ankle joint angle at maximum passive dorsiflexion or at the resting ankle angle (max. passive dors: R2adj ¼ 0:057, p = 0.673; resting ankle angle: R2adj ¼ 0:041, p = 0.22) (Fig. 2).
Normalised Muscle Length
0.75
0.7
0.65
0.6
0.55
0.5 0
0.5
1
1.5
2
2.5
2/3
Normalised Muscle Volume
Fig. 1. The relationship between normalised MG volume raised to the power of 2/3 and normalised MG length for the affected limb of children with SHCP (filled circles) and for TD children (open squares).
Normalised MG length
0.9 0.8 0.7 0.6 0.5 0.4 0.3 -60
-50
-40
-30
-20
-10
0
10
20
Ankle Angle (o) Fig. 2. The relationships between normalised muscle length and ankle angle at maximum passive dorsiflexion (open diamonds) and at the resting ankle angle (closed triangles).
4. Discussion We measured the MG volume, belly length, fascicle length and DFA in the affected and unaffected limbs of children with SHCP, and in a group of TD children. The affected limbs of children with SHCP demonstrated limited passive dorsiflexion range and greatly plantar flexed resting ankle angles. Our expectation that the MG of paretic limbs in SHCP would be shorter and smaller than in non-paretic and TD limbs was met, and our hypothesis that the shortness of the MG could not be explained by a reduction in fascicular length was proven. Normalised fascicle lengths in the paretic limbs were not significantly different to those in the limbs of TD subjects or in the non-paretic limb and the mean values were similar. Importantly, there was a significant relationship between normalised MG volume and normalised MG length in the affected limb of SHCP indicating that the fixed shortness of the MG belly is related to the failure of volumetric muscle growth. Intriguingly, muscle length in the affected limb, as measured by 3D ultrasound, was not related to the passive ankle dorsiflexion range or resting ankle angle. It is difficult to reconcile some of the differences we observed in the architecture and morphology of the MG in the non-paretic limb to TD muscle. Normalised MG volumes in the non-paretic limb were similar to those of the TD subjects but the muscles were significantly shorter at the resting angle. This could not be explained by a reduction in fascicular length and/or an increase in DFA as might be expected if we consider the MG to have parallelogram planar symmetry. It is possible that there are subtle differences in the 3D shape of the muscle that allows an altered distribution of fascicle lengths and angles for a given muscle length. While the small differences between non-paretic and typically-developing muscle are of interest they are unlikely to be of clinical importance. 4.1. Limitations of the study This paper relies on the assumption that the resting ankle angle with the knee extended equates approximately to the resting length of the muscle (gastrocnemius). In fact, a small tensile force will be exerted on the plantar flexors by the mass of the foot acting around the pivot of the ankle. The assumption may veer further from the truth if one of the other triceps surae is more involved than the MG, making the ankle more plantar flexed than by the MG alone. For additional discussions on this point see Yucesoy and Huijing (2007) and Huijing (2007). In addition, significant muscle activity in the plantar flexor or pretibial muscle groups could alter the resting angle during measurement. Although, we encouraged all the subjects to relax, we cannot guarantee the muscles of the calf were electrically silent. If either of these error conditions were significant, then the results concerning belly length at this resting ankle angle may carry less importance. This work may be criticised for not including a measurement of morphology at a refer-
Table 3 A fragment of the results (table from Shortland et al., 2002) Ankle joint angle (°) 30 Fascicle length (mm) Typically developing children Children with SDCP Normalised fascicle length Typically developing children Children with SDCP
Resting ankle position
36.1 ± 6.3 38.3 ± 11.5
37.4 ± 10.1 31.8 ± 9.8
0.126 ± 0.022 0.148 ± 0.042
0.130 ± 0.036 0.118 ± 0.031
The original and normalised results for fascicle length at a common angle, and at the resting ankle angle, are illustrated.
a
140 120
661
100 80 60 40 20 0 0
10
20
30
40
50
60
Body Mass (kg)
Muscle Length (mm)
b
300 250 200 150 100 50 150
200
250
300
350
400
350
400
Fibular length (mm)
c
70
Fascicle Length (mm)
ence or common ankle angle. Our reasoning for excluding these measures follows. The children with SHCP studied here represent a group with diverse resting ankle angles and angles of maximum passive dorsiflexion. A common ankle angle to both TD and SHCP groups would be in the order of 30° of plantar flexion. This angle would represent mechanically different states in the MG of affected and unaffected limbs: in TD children the MG would be in an unloaded state, while most of the muscles in the affected limbs of children with SHCP would be under stretch (please refer to Table 1). This is illustrated from our historical data collected on subjects with SDCP and with no pathology, using 2D ultrasound (Table 3; Shortland et al., 2002). The length of fascicles in TD children were very similar at the resting angle and a common ankle angle (30° of plantar flexion) while in children with SDCP the fascicle lengths were significantly longer at the common angle. The inclusion of a common angle may be valuable in a study of children with milder deformities. Under these circumstances, a common angle may be found in which the musculature is place under stretch in both affected and TD groups. Our results are limited to describing the morphology of the MG. It is possible that the morphology of different muscles in the paretic limb is altered according to their function and position within the musculoskeletal system. Recently, a study by Lampe et al. (2006) demonstrated that all the principal muscles in the paretic limbs of a group of young adults with SHCP were smaller than in the nonparetic limb. Using MRI, they found that the muscles of the thigh were more voluminous when compared to those in the non-paretic limb than the muscles of the leg (tibial segment). They reported a similar reduction in the volume of the gastrocnemius when compared to the unaffected limb to that reported here. This paper assumes that normalisation of muscle and fascicle length to skeletal length and muscle volume to body mass minimises the non-clinical variation in these parameters. Fig. 3a and b depicts strong relationships between muscle belly length at the resting ankle angle and fibular length (simple linear regression: R2adj ¼ 0:91, p < 0.00001), and muscle volume and body mass (R2adj ¼ 0:67, p = 0.00032), amongst the TD subjects. However, although there was a significant relationship between fascicle length and fibular length (p = 0.015), Simple linear regression analysis demonstrates that only 37% of fascicle length in
Muscle Volume (cm3)
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60 50 40 30 20 10 0 150
200
250
300
Fibular length (mm) Fig. 3. The relationship between resting muscle dimensions and selected anthropometric variables for TD children and (open squares) the affected limb of children with SHCP (closed circles): (a) muscle volume vs. body mass; (b) muscle length vs. fibular length; (c) muscle fascicle length vs. fibular length.
the TD group is explained by fibular length (Fig. 3c). It is possible that other anthropometric variables influence fascicle length in TD populations including the magnitude of the moment arms that the MG crosses. These relationships could be delineated with larger numbers of subjects and a suitable method for measuring a number of anthropometric variables including moment arms (Maganaris et al., 2006). As for TD muscle, much of the variation in volume and length of the MG in the paretic limb is explained by body mass (R2adj ¼ 0:63, p = 0.00025) and fibular length (R2adj ¼ 0:62, p = 0.00046), respectively (Fig. 3a and b). However, we could find no significant relationship between fascicular length and fibular length in the MG of the affected limb (p > 0.05) (Fig. 3c).
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4.2. Clinical implications Our main results have implications for understanding the relationship between muscle deformity and function in children with SHCP. A number of workers have measured the voluntary strength of the calf muscles in children with SCP (Elder et al., 2003; Stackhouse et al., 2005). The deficits in force production reported were attributed, in part, to the reduced voluntary activation of this muscle group, and to the coactivation with antagonist muscle groups. Our findings suggest that a large proportion of the weakness of the calf musculature is caused by a mechanical deficit related to a significant reduction in volume. It is likely that deleterious changes to muscle fibres and the proliferation of the extracellular matrix also contribute to the poor mechanical function of muscle in this group (Booth et al., 2001; Lieber et al., 2003). Our results indicate that the failure of growth of the affected muscle was not caused by short fascicles but by a reduction in cross-section (Fig. 1). The origins of these differences at the cellular level are unclear but it is possible that a reduction in muscle fibre diameter (Lieber et al., 2003) and/or a reduction in the number of fibres (through premature cell death) is responsible. The relationship between the passive range at a joint and the dimensions of the muscle bellies crossing that joint has not been studied to our knowledge. The children with SHCP in this study presented with a wide range of limitations in maximum passive ankle dorsiflexion and a wide range of muscle volumes and lengths. Importantly, we did not find a relationship between normalised muscle length and ankle angle at the resting angle or maximum dorsiflexion (Fig. 2). This study included a limited number of ambulant children and measurements were made on a single muscle so care needs to exercised in extrapolating our results to the other muscles in the lower limb. However, if the poor relationships between joint range and muscle dimensions are confirmed for other muscles and joints then we may have to consider musculotendinous shortness (limited passive range) and muscle belly deformity (reduced muscle volume) as distinct phenomena in the child with SHCP. Acknowledgements Nicola Fry was supported by an Award from the National Co-ordinating Centre for Research Capacity Development (UK). Anne McNee was supported by award from Sports Aiding Medical Research in Kids (SPARKS). References Booth CM, Cortina-Borja MJ, Theologis TN. Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol 2001;43(5):314–20. Bottos M, Feliciangeli A, Sciuto L, Gericke C, Vianello A. Functional status of adults with cerebral palsy and implications for treatment of children. Dev Med Child Neurol 2001;43(8):516–28. Elder GC, Kirk J, Stewart G, Cook K, Weir D, Marshall A, et al.. Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol 2003;45(8):542–50.
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Anne McNee MPhty is a Research Physiotherapist in the Paediatric Neurosciences Unit in Guy’s & St. Thomas’ Foundation Hospital Trust. Anne is interested in the effect of immobilisation therapy, botulinum toxin and strengthening on the morphology of muscles. She is currently conducting a population study on the relationship between deformity, function and quality of life in older children and young adults with bilateral cerebral palsy.
Dr. M Gough MCh FRCS(Orth), Consultant Paediatric Orthopaedic Surgeon, Guy’s and St. Thomas NHS Foundation Trust, London. He has a special interest in the orthopaedic management of children with neuromuscular deformity, and research interests in the natural history of deformity, its effect on function, and the effect of intervention.
Nicola Fry MSc, Research Clinical Scientist at One Small Step Gait Laboratory, Guy’s & St. Thomas’ NHS Foundation Trust, London. Nicola has developed a 3D ultrasound technique for measuring the volume of muscles and has undertaken research projects which utilise this technique. She is currently working towards her PhD looking at musculo-skeletal deformity in cerebral palsy.
Adam Shortland PhD, Consultant Clinical Scientist and Gait Analysis Service Manager at Guy’s & St. Thomas NHS Foundation Trust and Honorary Senior Lecturer, King’s College, London. His pre-doctoral and postdoctoral studies included ultrasound imaging, biofluid dynamics, muscle mechanics and biomaterials at Sheffield and Liverpool University Medical Schools, UK. He is currently researching the musculoskeletal mechanisms for declining mobility in children with spastic cerebral palsy. Presently, Chairman of the Rehabilitation Engineering and Biomechanics Special Interest Group of the Institute of Physics and Engineering in Medicine (UK).
Linda Eve MCSP, clinical specialist physiotherapist, trained at the London Hospital and specialised in paediatrics with a special interest in cerebral palsy. She worked at the Cheyne Centre for Spastic Children, and was involved with the identification of levels of ability at this centre. She worked in community paediatrics before taking on her current post at the One Small Step Gait Laboratory at Guy’s & St Thomas’ NHS Foundation Trust. Here she has been involved in investigating kinetics in assisted ambulation and has also contributed to setting standards in gait analysis for the clinical laboratories in the UK.