Muscle strength and walking ability in Diplegic Cerebral Palsy: Implications for assessment and management

Gait & Posture 33 (2011) 321–325

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Muscle strength and walking ability in Diplegic Cerebral Palsy: Implications for assessment and management Nicky Thompson a,b,*, Julie Stebbins a, Maria Seniorou a, Di Newham b a b

Oxford Gait Laboratory, Nuffield Orthopaedic Centre, Oxford, UK Division of Applied Biomedical Research, King’s College, London, UK

A R T I C L E I N F O

A B S T R A C T

Article history: Received 5 March 2010 Received in revised form 13 August 2010 Accepted 5 September 2010

Muscle weakness is a recognised problem in children with Cerebral Palsy (CP). Changes in the understanding of motor control, and progress in the treatment of spasticity, have led to a greater appreciation that spastic muscles are also weak. In recent years weakness has been identified in isolated muscle groups, but studies quantifying the degree and distribution of weakness in multiple muscles remain limited. This study evaluated isometric lower limb muscle strength in 50 ambulant children with CP/Spastic Diplegia (mean age 11 years 7 months) at GMFCS levels I (n = 14), II (n = 26) and III (n = 10). Muscle strength was compared with 15 control children (mean age 11 years 1 month) using the same protocol. Six muscle groups in both lower limbs were measured using a digital dynamometer. All lower limb muscles were significantly weaker in the CP children than in healthy children (p < 0.05) except for the hip extensors. Muscle strength ranged from 43% to 90% of control values depending on the muscle group, with the knee extensors measured at 308 being the relatively weakest group. There was a significant difference in strength between GMFCS levels in 4/6 muscle groups with a progressive reduction in strength in all muscle groups with increasing walking difficulty from GMFCS levels I to III. The greatest difference in strength between independent walkers and those dependent on walking aids was in the hip abductors and knee extensors at 308, which are key muscle groups in sagittal and coronal plane walking stability. This has implications in targetting strength training to maximise functional outcomes. ß 2010 Elsevier B.V. All rights reserved.

Keywords: Cerebral Palsy Muscle strength Gross motor functional classification system Gait

1. Introduction Children with spastic Cerebral Palsy (CP) have smaller [1,2] and weaker muscles [3,4] than healthy children. Muscle strength correlates with gait [5,6] and motor function [7] and strength is more highly related to function than spasticity [6]. Spastic muscles respond positively to strength training and strength gains have been shown to be similar or greater than those reported in the healthy population [8]. Various studies have reported significant improvements in gait following strengthening programmes in terms of temporal parameters [7,9,10] and Gross Motor Function Measure (GMFM) Dimension E [7,10–12]. McPhail and Kramer [8] found a direct correlation between the strength gained and functional improvement, but significant changes in gait kinematics following strength training appear difficult to achieve and have rarely been reported [11]. These strengthening studies, however,

* Corresponding author at: Oxford Gait Laboratory, Nuffield Orthopaedic Centre NHS Trust, Oxford OX3 7LD, UK. Tel.: +44 01865 227609. E-mail address: [email protected] (N. Thompson). 0966-6362/$ – see front matter ß 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2010.10.091

presume weakness is present, and reports specifically documenting the extent and distribution of muscle weakness in children with CP remain very limited. In Spastic Diplegia (SD), the most prevalent diagnostic category of CP, muscle strength has been quantified at the knee joint [13], and two lower limb strength profiles have been undertaken and compared with controls [3,4]. The purpose of this study was to examine the extent and distribution of weakness in lower limb muscles in SDCP in comparison to a healthy control group and to relate this to ambulatory function. The intention was to help progress our understanding of which muscle groups play an important role in achieving independent ambulation, and may also serve as a basis for planning management and improving functional outcomes. 2. Patients The participants in this study were 50 children (28 boys, 22 girls) with an established diagnosis of SDCP and mean age of 11 years 7 months (range 7 years 1 month–16 years 9 months) who walked with or without walking aids. Using the Gross Motor Function Classification System (GMFCS) [14] 14 children were

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classified as level I, 26 children as level II and 10 children as level III. Patients had no orthopaedic surgery or Botulinum toxin in the year preceding the study and, at the time of assessment, were on the waiting list for single event multi-level surgery (SEMLS). A group of 15 healthy children (seven boys, eight girls) with no known neurological or orthopaedic problems and mean age 11 years 1 month (range 7 years–15 years 1 month) were recruited as controls. Children were excluded below the age of 5 years, since it was assumed they could not consistently perform isometric strength testing, and over the age of 18 years. 3. Methods Each CP child underwent a clinical examination including range of motion measurements and manual muscle testing of the lower limbs. Maximal isometric muscle strength was measured in all children in six muscle groups in each leg using a digital myometer (MIE Medical Research Ltd., Leeds, UK) sampling at 50 Hz. The myometer was calibrated prior to each assessment. Muscle groups measured were: the hip flexors, extensors and abductors, the knee flexors, and the knee extensors at both 308 and 908 of flexion. Each child was tested in standardised positions (Table 1) and muscle groups tested sequentially. The positions were based on the existing strength testing literature [15] in gravity neutral positions as possible. The child was instructed to hold onto the couch in both sitting and lying, and pelvic stabilisation was used to minimise compensatory movements. A combination of fixed and hand-held techniques were used; fixed dynamometry was used for the knee extensors where normal values were expected to exceed the upper limb strength of the assessor using a hand-held technique. Maximal isometric contractions were performed using a ‘make test’, which maintains the muscle at a constant length to minimise eliciting a reflex during the test [16]. The technique was clearly explained and a practice trial undertaken at the start of the session to familiarise the child with the technique. Three trials were administered and recorded for each muscle group and strong verbal encouragement was used during the trial to achieve maximum effort. We have previously undertaken a reliability study of the above protocol in 5 children with SDCP CP/Spastic Diplegia and 5 healthy children [17]. The same assessor repeated testing of all six muscle groups over three visits held at least one week apart. Two assessors each repeated testing of three muscle groups over three visits held at least one week apart. The protocol demonstrated very good intra- and inter-rater reliability for the isometric strength testing in the healthy group (ICC > 0.81) and good reliability for the CP group (ICC > 0.61). The rate of maximal

force development and maximal voluntary contraction force was reduced in the CP children, which is consistent with the literature [18]. 3.1. Data analysis Isometric muscle strength was expressed as torque (Nm) by multiplying the force measurements by the lever arm distance. This was the distance from the estimated joint centre of rotation to the point of application of the force, measured with a tape measure (Table 1). The peak value for each muscle group was normalised to body mass (Nm/kg) and used for analysis. Differences in mean muscle strength values between the CP and control groups were analysed using an independent t-test (p < 0.05). Differences in both mean muscle strength values and mean joint angles according to walking ability (GMFCS level), were analysed with one-way analysis of variance (ANOVA) and Tukey post hoc testing (p < 0.05) using SPSS version 16 (SPSS Inc., Chicago, IL). Not all data could be obtained. The maximum force limit of the MIE myometer is 1000 N but hip extensor strength sometimes exceeded the upper limb strength of the assessor (450 N). Where this occurred, in 8/30 control limbs and in 2/100 CP limbs, a value of 450 N was ascribed for analysis. Some children had insufficient hip abductor strength to register a reading on the myometer. This occurred in 11/100 CP limbs and a value of 0 N was ascribed for analysis. It was not possible to measure the strength of the knee extensors at 308 in 26/100 CP limbs due to knee flexion contractures and these were excluded from the analysis.

4. Results Mean joint angles and mean maximal normalised strength values for all test positions in all CP children versus controls, as well as CP children according to GMFCS level, are shown in Table 2. Muscle strength in the CP children was significantly less than controls in all muscle groups with the exception of the hip extensors. Fig. 1 shows the strength profile of the CP children with mean strength values presented as a percentage of control values. Muscle strength of the CP children ranged from 43% to 90% of control values depending on the muscle group. The knee extensors measured at 308 of flexion was the relatively weakest muscle group. With worsening ambulatory level from GMFCS levels I to III strength values decreased incrementally in all muscle groups,

Table 1 Standardised positions for strength testing protocol. Figure

(

Muscle group

Subject position

Dynamometer position

Lever arm distance

Hip flexors

Supine

Hip and knee flexed to 908. Thigh cuff around distal thigh, proximal to femoral condyles. Dynamometer held so hip flexion is resisted

Greater trochanter to thigh cuff

Hip extensors

Supine

Hip and knee flexed to 908. Thigh cuff around distal thigh, proximal to femoral condyles. Dynamometer held so hip extension is resisted

Greater trochanter to thigh cuff

Hip abductors

Supine

Hip and knee flexed to 308 in near neutral abduction. Thigh cuff around distal thigh, proximal to femoral condyles. Dynamometer held so hip abduction is resisted

Greater trochanter to thigh cuff

Knee flexors

Sitting

Hip and knee flexed to 908. Ankle cuff around distal leg, proximal to malleoli. Dynamometer held so that knee flexion is resisted

Lateral femoral condyle to ankle cuff

Knee extensors 908

Sitting

Hip and knee flexed to 908. Ankle cuff around distal leg, proximal to malleoli. Dynamometer fixed to a stable point so knee extension is resisted

Lateral femoral condyle to ankle cuff

Knee extensors 308

Sitting

Hip flexed to 908 and knee to 308. Ankle cuff around distal leg, proximal to malleoli. Dynamometer fixed to a stable point so knee extension is resisted

Lateral femoral condyle to ankle cuff

) Fixed point. ( ) Direction of active muscle contraction. ( ) Direction of resistance.

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Table 2 Mean (SD) joint angles (8) and normalised muscle torque values (Nm/kg) of all CP children versus controls and for CP children according to GMFCS. ‘n’ represents number of legs in each group. Bold type indicates significant difference between CP and control children.

Mean age (range) Joint angles (8) Hip flexion contracture Knee flexion contracture Popliteal angle Normalised torque (Nm/kg) Hip flexors Hip extensors Hip abductors Knee flexors Knee extensors at 908 Knee extensor at 308

Controls (n = 30)

CP (n = 100)

GMFCS I (n = 28)

GMFCS II (n = 52)

GMFCS III (n = 20)

11.1 (7.0–15.1)

11.7 (7.1–16.9)

12.1 (8.6–16.9)

11.6 (7.1–15.4)

11.2 (7.9–15.1)

7 (8) 4 (14) 65 (17)

6 0 57

7 4 65

12a,b 10a 77a,b

0.02 0.06 <0.001

0.47 2.18 0.31a,b 0.83a 1.21a 0.42a,b

0.49 0.17 <0.001 0.01 0.001 <0.001

1.05 2.64 1.05 1.26 1.82 1.27

(0.19) (0.51) (0.29) (0.25) (0.37) (0.17)

0.51 2.37 0.61 0.93 1.50 0.56

(0.21) (0.83) (0.23) (0.28) (0.54) (0.30)

p value

<0.001 0.10 <0.001 <0.001 0.03 <0.001

0.55 2.62 0.79 1.05 1.78 0.77

0.51 2.32 0.53c 0.89c 1.46c 0.45c

p value

Muscle Strength (% Control)

p value indicates level of significance for the ANOVA analysis between all three GMFCS levels. a Significant difference between GMFCS levels I and III. b Significant difference between levels II and III. c Significant difference between GMFCS levels I and II.

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5. Discussion

120 100 80 60 40 20 0 Hip Flex

Hip Ext

Hip Abd

Knee Flex Knee Ext 90 Knee Ext 30

Muscle Group Fig. 1. Lower limb muscle strength profile of 50 CP/SD children presented as a percentage of healthy values.

while joint contractures increased (Fig. 3 and Table 2). ANOVA analysis revealed a significant difference in muscle strength between GMFCS levels in four out of six muscle groups and post hoc analysis showed this difference to be between GMFCS levels I and II, and levels I and III in the four muscle groups and between levels II and III in two muscle groups. The greatest strength reduction between independent (GMFCS level I) and dependent walkers (GMFCS level III) was in the hip abductors (61%) and knee extensors at 308 (45%).

The degree and distribution of weakness in children with CP/SD has not been well documented. The finding of lower limb weakness in all muscle groups tested, when compared with controls, is in agreement with the two existing strength profiles in Diplegic CP [3,4]. We measured a range of 43–90% of control values depending on the muscle group. It is however difficult to observe distinct trends in the extent or pattern of weakness between this and the existing two strength profiles, due to differences in the age range, muscles measured, testing position, technique and analysis. In particular, these three studies highlight that muscle strength is position dependent. The optimal position for measuring muscle strength is a gravity-neutral position to eliminate the effect of the weight of the limb, which will vary subject to subject, and to facilitate the measurement of subjects with sub-gravity strength. In all three studies the only muscles measured in identical gravityneutral positions were the hip abductors and knee extensors at 908 and these show remarkably similar readings when expressed as a percentage of control values (Fig. 2). Eek et al. [19] chose to measure the hip flexors and knee flexors in both anti-gravity and gravity-neutral positions, and the hip extensors in two different anti-gravity positions, but then combined the two measurements for each muscle group in the analysis. They reported significantly higher values for controls in the hip flexors in sitting (anti-gravity) versus supine lying (gravity neutral), significantly higher values for the knee flexors in sitting (gravity neutral) versus prone lying

Fig. 2. Isometric lower limb strength in children with SDCP—comparison of the findings of this study with existing published strength profiles. Strength values are expressed as a % of control values.

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(anti-gravity) but no significant difference for the hip extensors. It is therefore likely there is some overestimation of hip flexor strength and underestimation of knee flexor strength in CP subjects as a percentage of normal in this group [4] compared to ours, which if taken into consideration may bring these readings closer to the results from this study and Wiley and Damiano [3]. The hip extensors are a particularly problematic group to measure accurately. Crompton et al. [20] have shown it is possible to measure this muscle group reliably in supine lying but not in prone. We deliberately chose supine lying with the hip and knee flexed as a gravity-neutral position, and to isolate gluteus maximus from the hamstrings. Hip extensor strength in this position is considerably greater than in prone lying [20]. This may be due to some additional contribution from the hamstrings and possibly knee extensors working in concert. Frigo et al. [21] suggest cocontraction of the knee extensors and hamstrings may be a well coordinated compensation for hip extensor weakness, rather than a pathological action. It is, however, interesting to note that the gluteus maximus in Lampe et al.’s [1] study of hemiplegic subjects were close in volume to the unaffected side. The alternative use of anti-gravity positions in prone, with and without isolating gluteus maximus, by Wiley and Damiano [3] and Eek et al. [4], respectively, restricted the number of patients who could achieve this starting position due to weakness. All three studies may therefore have over estimated the strength of the hip extensors due to these difficulties. We found an incremental reduction in strength in all muscle groups with increasing walking difficulty from GMFCS levels I to III (Fig. 3) as did Eek and Beckung [22]. Mean ages and age ranges were similar across GMFCS levels with no significant difference in age between GMFCS levels. The greatest drop in strength between independent ambulators (GMFCS level I) and those dependent on walking aids (GMFCS level III) was in the hip abductors (61%) and the knee extensors at 308 (45%). Eek et al.’s data also showed the greatest drop in strength between GMFCS levels I and III to be in the hip abductors as well as the hip extensors. They did not however measure the knee extensors at 308. These proximal muscle groups are key groups in maintaining dynamic stability during gait. Throughout stance muscles contract when body alignment creates an external moment which threatens the weight-bearing stability of the limb and trunk. In the sagittal plane the moments that must be controlled are those that induce hip flexion, knee flexion and ankle dorsiflexion. In the coronal plane the effects of gravity predominantly induce an external hip adductor moment which threatens the stability of the pelvis and

trunk. These two studies highlight a significant loss of strength in the hip extensors, knee extensors and the hip abductors with increasing GMFCS classification and these are key muscle groups associated with sagittal and coronal plane stability during independent walking. Targetting key muscle groups in strength training programmes to maximise walking ability is an important consideration during routine therapy treatment, during rehabilitation following surgery, as well as targeted sparing of muscle strength during surgery [23]. Multiple impairments contribute to motor deficits in CP. We did not evaluate muscle strength at the ankle which we found difficult due to impairment of selective voluntary motor control distally combined with foot deformity in some children. Crompton et al. [20] have shown large variability when measuring the ankle plantarflexors in CP children and testing of these muscles with hand-held dynamometry is unreliable. Furthermore, in healthy children we found the plantarflexors difficult to manually stabilise due to the short lever arm and very high force generating capacity. This is a limitation of this study since CP children demonstrate significant power deficits in the ankle plantarflexors during gait. Wiley and Damiano did use hand-held dynamometry but included children who were unable to achieve a neutral ankle position [3], while Eek et al. built a special device to stabilise the dynamometer and measure the plantarflexors [19]. Both found the ankle dorsiflexors to be one of the weakest groups in SDCP but it would be helpful to separate out the influence of selective control and foot deformity. Objective assessment of selective voluntary motor control has been a challenge but Fowler’s recently validated ‘Selective Control Assessment of the Lower Extremity’ (SCALE) is a promising new tool [24]. In the 1990s there was a resurgence of interest in strength training in children with CP and initial studies concentrated on establishing whether it was possible to strengthen muscles in this group of patients. Progressive strength training has since been shown to result in moderate to large gains in both strength and function but relatively mild changes in gait [25]. Only recently have studies begun to emerge which target resistance strengthening to specific muscle groups. Engsberg and Ross [11] and McNee et al. [26] focused solely on the distal musculature. Engsberg and Ross [11] randomised 12 CP/SD children to a 12 weeks of isotonic strength training of the dorsiflexors, or plantaflexors, or dorsi and plantarflexors and evaluated gait and motor function. McNee et al. [26] evaluated a 10-week resistance programme for the plantarflexors on 13 hemiplegic and diplegic children and looked at the effect on in muscle volume, gait and motor function. Eek et al. [4]

Fig. 3. Normalised muscle strength in the lower limbs of SDCP children for GMFCS levels I–III, compared with controls.

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assessed whether an 8-week strength training programme could specifically influence the gait pattern and gait function of 16 CP/SD children by training four lower limb muscle group chosen on the basis of strength testing and gait abnormality (kinematics and kinetics). Damiano et al. [27] examined whether 8 weeks of progressive strength training of the hip and knee extensors could diminish the degree of crouch and internally rotated gait in 8 children with spastic Diplegic CP. So far the outcomes of these more focused studies remain equivocal, with significant improvements in strength or muscle volume in all studies, significant improvement in motor function in two [4,11] out of four studies, significant improvement in just one kinematic parameter in one study [11], and no significant improvement in temporal parameters in any of the four studies. The absence of improvement in gait kinematics in Eek et al.’s [4] study was perhaps not surprising given the variability in target muscles which were strengthened across subjects. However, this was the only study to additionally measure kinetics which did show significant improvements in hip extensor moments and ankle power. Their subjects included independent ambulators only (GMFCS levels I and II), while the remaining studies included independent ambulators as well as those at a lower functional level using assistive devices (GMFCS levels I–III). Damiano et al. [27] undertook a sub-group analysis comparing independent ambulators with those with assistive devices. The children who were more functional showed a small improvement in crouch in comparison with an appreciable worsening in the children who required assistive devices to walk. This still did not reach statistical significance but the numbers were small. We have also found that GMFCS level II subjects respond significantly better to strength training than GMFCS level III [28]. Mockford and Caulton’s [25] recent systematic review of strength training in CP found more conclusive results than other reviews [29,30] by deliberately limiting the clinical heterogeneity of CP to ambulatory children and adolescents and excluding upper limb studies, adults and non-ambulatory subjects. They concluded that function and gait improve more in younger than older subjects. We need to consider how to further improve the outcomes of future strength studies by reducing the heterogeneity of CP by not only focusing strength training to target muscles but evaluating results by subgroups such as functional or GMFCS level and age. This study confirms that ambulant children with Diplegic CP, even those who are mildly affected, have significant lower limb weakness when compared with controls. We found an incremental drop in strength in all muscle groups with increasing walking difficulty, from GMFCS levels I to III. The greatest drop in strength between independent ambulators and those needing assistive devices was in the hip abductors and knee extensors at 308 which are key muscle groups in sagittal and coronal plane walking stability. This has implications in targetting strength training to maximise functional outcomes. The study highlights important considerations in the assessment of muscle strength to reflect true readings of individual muscle groups and to facilitate comparison of strength outcomes across studies.

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