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Gait & Posture 38 (2013) 1038–1043

Contents lists available at SciVerse ScienceDirect

Gait & Posture


journal homepage: www.elsevier.com/locate/gaitpost

The relationship between clinical measurements and gait analysis data


in children with cerebral palsy
Małgorzata Domagalska a,*, Andrzej Szopa a, Małgorzata Syczewska b,
Stanisław Pietraszek c, Zenon Kidoń c, Grzegorz Onik a
a
Faculty of Health Sciences, Medical University of Silesia, Katowice, Poland
b
Paediatric Rehabilitation Department, The Children’s Memorial Health Institute, Warszawa, Poland
c
Institute of Electronics, Silesian University of Technology, Gliwice, Poland

A R T I C L E I N F O A B S T R A C T

Article history: Spasticity is a common impairment that interferes with motor function (particularly gait pattern) in
Received 7 December 2012 children with cerebral palsy (CP). Gait analysis and clinical measurements are equally important in
Received in revised form 20 May 2013 evaluating and treating gait disorders in children with CP. This study aimed to explore the relationship
Accepted 27 May 2013
between the spasticity of lower extremity muscles and deviations from the normal gait pattern in
children with CP. Thirty-six children with spastic CP (18 with spastic hemiplegia [HS] and 18 with spastic
Keywords: diplegia [DS]), ranging in age from 7 to 12 years, participated in the study. The children were classified as
Cerebral Palsy
level I (n = 24) or level II (n = 12) according to the Gross Motor Function Classification System. Spasticity
Clinical assessment of spasticity
Accelerometer
levels were evaluated with the Dynamic Evaluation of Range of Motion (DAROM) using the
Gait accelerometer-based system, and gait patterns were evaluated with a three dimensional gait analysis
Gillette Gait Index using the Zebris system (Isny, Germany). The Gillette Gait Index (GGI) was calculated from the gait data.
The results show that gait pathology in children with CP does not depend on the static and dynamic
contractures of hip and knee flexors. Although significant correlations were observed for a few clinical
measures with the gait data (GGI), the correlation coefficients were low. Only the spasticity of rectus
femoris showed a fair to moderate correlation with GGI. In conclusion, the results indicate the
independence of the clinical evaluation and gait pattern and support the view that both factors provide
important information about the functional problems of children with CP.
ß 2013 Elsevier B.V. All rights reserved.

1. Introduction The Dynamic Evaluation of Range of Movement (DAROM) is an


assessment that considers spasticity, dependence on movement
Various treatment strategies are used to improve motor velocity, and the position of adjacent joints. The instrument was
function in children with cerebral palsy (CP). Clinical examination introduced by Reimers and Jóźwiak [9–11]. The reliability of the
combined with gait analysis is often used to assess the effective- Ashworth Scale has been questioned [8]. The MTS and the DAROM
ness of various treatment methods [1–8]. The most popular (a simplification of the MTS), which uses at least 2 different
methods of clinical muscle tone assessment are subjective scales, velocities of passive muscle stretching, have reported satisfactory
including the Ashworth Scale (AS), the Modified Ashworth Scale intra- and inter-rater reliability [2,8]. However, these assessments
(MAS), the Tardieu Scale (TS), and the Modified Tardieu Scale (MTS) are not objective tests. The DAROM, similar to the MTS, defines the
[2,8]. In children with spastic CP, there is a strong correlation ROM as slow and fast passive stretching to determine a dynamic
between the range of motion (ROM), the velocity of movement, component of muscle contracture [2,10,11]. In contrast with a
and the position in which the tested muscle reacts to stretching standard clinical examination, the DAROM identifies a ‘‘range of
[2,9–13]. motion deficit’’ (DROM), defined as a value from the minimal
muscle stretch position. In this test, two joint angles are measured:
DROM I, defined as the PROM deficit following a slow velocity
stretch, and DROM II, defined as the angle of catch (AOC) after a fast
* Corresponding author at: Faculty of Health Sciences, Medical University of velocity stretch. The difference between DROM II and DROM I
Silesia, Medyków 12, 40-752, Katowice, Poland. Tel.: +48 601 516 725;
indicates the examined muscle group’s level of contracture and is
fax: +48 322088712.
E-mail addresses: mdomagalska@sum.edu.pl (M. Domagalska), called the angle of spasticity (ASO) [2,10–13]. The DAROM, again
aszopa@sum.edu.pl (A. Szopa). like the MTS, specifies three velocities that can be applied to the

0966-6362/$ – see front matter ß 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.gaitpost.2013.05.031
M. Domagalska et al. / Gait & Posture 38 (2013) 1038–1043 1039

muscle [12]: V1, as slow as possible; V2, the speed of the body orthopaedic problems and mean age of 8 years and 8 months
segment falling freely under gravity; and V3, as fast as possible. In (range: 7 years, 5 months to 12 years, 3 months) was recruited as a
the DAROM, the precise measurement of a limb’s position during reference group (Ref). These children underwent only gait analysis.
testing is essential [9–11].
Currently, one of the most commonly used methods for 2.2. Testing procedure
assessing motor deficits in children with CP is objective,
instrumented gait analysis. An algorithm called bridge therapy Each child with CP underwent a clinical examination, including
is often used: in this algorithm, spasticity and contracture are DAROM, of the four muscle groups in each leg. The testing positions
managed simultaneously using orthotic devices [3–7,13–16]. and standardisation procedures for all measurements are shown in
However, while most gait analysis reports are based on selected Table 1. All of the measurements were performed at the functional
gait parameters [3–7], many gait parameters are interdependent. testing lab of the University of Silesia. All of the participants were
Moreover, improvements in selected gait parameters are not examined three times (on consecutive days) by the same well-
always equal to global gait pattern enhancement. To overcome trained physiotherapist. The child was instructed to hold onto a
these problems, an index for quantifying deviations from normal couch in both sitting and lying positions, and the pelvis was
gait, called the Gillette Gait Index (GGI) and, previously, the stabilised to minimise compensatory movements. The therapist
Normalcy Index (NI) [17], was introduced. This index is a global moved the segment of the lower limb from the starting position
measure of gait pattern based on 16 selected gait parameters taken towards the final position at two velocities (V1 and V3), holding the
from objective gait analysis. However, data comparing the limb at the end of the available range while testing with the slow
spasticity determined via quantitative clinical examination with velocity (DROM I) or at the position of the AOC (DROM II) while
the results of objective gait analysis are scarce in the literature. testing with the fast velocity.
Therefore, the purpose of this study was to explore the
relationship between spasticity in the muscles of the lower 2.3. Data collection and analysis
extremities, assessed with the DAROM method, and deviations
from normal gait in children with CP. The DROM I and DROM II angles were measured (in degrees)
using an accelerometer-based system with ZK software (Institute
2. Methods of Electronics of Silesian University of Technology) [19]. The limb
segment coordinates were defined by external markers. The results
The research protocol was approved by the Bioethics Commit- from the three trials were averaged to obtain the DROM I and
tee of the Medical University of Silesia in Katowice, Poland. The DROM II values. The ASO value was calculated as the difference of
parents/guardians signed an informed consent form prior to the DROM II DROM I [3]. Angular velocity was measured using an
subjects’ enrolment into the study. accelerometer system.

2.1. Subjects 2.4. Three-dimensional instrumented gait analysis

Thirty-six children with CP, 18 with hemiplegia (HS) and 18 After clinical examination, objective gait analysis was per-
with diplegia (DS), were included in the study. All of the formed using the Compact Measuring System for 3D Real-Time
participants were independently functioning outpatients (Level I Motion Analysis (CMS- HS 3D) with WinGait software (Zebris
or II of the Gross Motor Function Classification System [GMFCS]) Medizintechnik GmbH, Germany). The CMS HS 3D system is based
[18] at local paediatric rehabilitation centres. The inclusion criteria on 15 active ultrasonic markers (five triplets of ultrasound
were a diagnosis of the predominantly spastic type of CP, the markers).[20]
ability to walk without assistive devices, age 7 to 12 years, Before gait analysis, the following anatomic landmarks were
sufficient cooperation to enable accurate clinical assessment and identified with an instrumented pointer: hip joint centre, knee
three-dimensional gait analysis, no surgeries within 18 months, rotation centre (internal and external), ankle rotation centre
and no inhibiting casts or botulinum toxin treatment 6 months (internal and external), forefoot landmark (between the second
before the evaluation. The HS group consisted of 6 girls and 12 and third metatarsals), and rear foot (heel). Gait data were
boys; deficits occurred on the right side in 12 patients and on the recorded while the subjects walked on an Alfa XL treadmill
left side in 6, and the mean age was 8 years and 2 months (range: 7 (Kettler, Germany). Prior to data collection, all subjects had the
years, 4 months to 12 years, 2 months). The DS group consisted of 8 opportunity to practice walking on the treadmill. The children
girls and 10 boys; the mean age was 10 years and 4 months (range: walked without shoes and without assistive devices. Markers were
8 years, 3 months to 12 years, 2 months). A group of 18 healthy attached to the skin with double-sided adhesive tape and placed
children (6 girls and 12 boys) with no known neurological or bilaterally. Depending on each subject’s walking abilities, five to

Table 1
Accelerometer placement and stabilisation for dynamic assessment of range of motion (DAROM tests).

Test Testing position Position of accelerometer Stabilisation

T1 Deficit of hip extension Supine, the contralateral extended leg resting 10 cm proximal to the lateral epicondyle femur, parallel Pelvis
in the Thomas test on a support to the long axis of the femur
T2 Pelvis elevation angle in Prone, both lower limbs extended resting on a support 10 cm distal to the trochanter major, parallel to the long Without
the Duncan-Ely test axis of the femur stabilisation
T3 Popliteal angle Supine, hip and knee of tested leg flexed 908, ankle in Anterior, 5 cm proximal to the lateral malleolus, parallel Pelvis
neutral position, contralateral flexion leg resting on to the long axis of the fibula
support
T4 Deficit of knee extension Supine, hip of tested leg in neutral position in all planes Anterior, 5 cm proximal to the lateral malleolus, parallel Pelvis
and knee flexed 908, off the table with the ankle in a to the long axis of the fibula
neutral position contralateral extended leg resting on
support
1040 M. Domagalska et al. / Gait & Posture 38 (2013) 1038–1043

eight gait cycles were recorded for further analysis. The GGI was significantly larger in each test than the average DROM of the
calculated separately for each leg using the procedure described by unaffected leg was. A main effect of muscle group was significant in
Schutte.[17] both groups of CP children, in HS F(3, 102) = 2.20, p = .001 and in DS
F(3, 105) = 10.48, p = .001. Each DAROM test (T1, T2, T3, T4)
2.5. Statistical analysis differed in the reported DROM (Table 2). A main effect of applied
velocity (V1, V3) was found in the HS (F(3, 102) = 12.53, p < .001)
The normality of the distribution of the analysed parameters and DS groups (F(1, 35) = 90.80, p < 001), with significantly larger
was assessed using skewness and kurtosis and Shapiro–Wilk’s test. DROM values in both groups when V3 was applied (Fig. 1). A main
Normally distributed variables were summarised as the means and effect of level of involvement was found for the lower limbs of
standard deviations; non-normally distributed variables are children with HS (F(2, 99) = 16.54 p < .001), indicating that the
presented as median and range. The DROM results were compared average DROM of the affected leg was significantly greater than
using a three-way repeated measure ANOVA. An alpha level of 0.05 that of the unaffected leg in each test. There was a significant
was chosen as a cut-off for all statistical comparisons, and interaction between main factors (F(3, 51) = 34.30, p < .001). Post
Bonferroni post hoc comparisons were performed when necessary. hoc analysis showed that DROM applied with V3 (DROM II) to the
ASO and GGI were compared using a one-way repeated measure unaffected hemiplegic leg was not different from DROM I (applied
ANOVA (for the different types of lower limbs). The biomechanical with V1) in each DAROM test. There was a significant interaction
parameters and GGI for hemiplegic patients were evaluated for the between main factors (F(2, 99) = 21.17, p < .001). The DROM
affected and unaffected sides separately; however, for the diplegic measured in the affected hemiplegic leg with V3 (DROM II) was
and control subjects, the data from the left and right legs were significantly larger than the DROM measured with V1 (DROMI),
pooled together. The correlation between GGI and all biomechani- but only in T3 and T4. In the diplegic legs, DROM II did not differ
cal parameters (DROM I, DROM II, ASO) was tested using a from DROM I in T3 and T4; however, in T1 and T2, DROM II was
Spearman rank correlation coefficient. The software package significant larger (Fig. 2A–C). A two-way analysis of variance
Statistica (Version 9.0 PL) was used for statistical analysis. yielded a main effect of lower limb involvement level (F(1,
34) = 91.70, p < .001), such that the average ASO was significantly
3. Results larger for the affected hemiplegic leg than for the unaffected leg in
each DAROM test, excluding T2. Additionally, the ASO for the
3.1. Data analysis of angular velocity measurements affected hemiplegic leg was significantly larger than the ASO of the
diplegic leg in the first and second DAROM test (F(1, 52) = 5.07,
The median and range of slow (V1) and fast (V3) angular p = .001), but it was not significantly larger in the third and fourth
velocity applied during DAROM depended on the test time point (Table 1). The interaction of main factors was significant
(T1, T2, T3, T4) and the type of lower limb tested (unaffected and (F(3,156) = 21.17, p = .001).
affected in children with HS and the affected legs of children with
DS). The fastest angular velocity (V3) was observed at T3 for the 3.3. Gillette Gait Index (GGI)
unaffected hemiplegic leg (147.24  37.968/s), while the slowest
angular velocity (V1) was observed in T2 in children with DS The level of lower limb involvement for the GGI is shown in
(24.14  7.348/s). The differences between the V1 and V3 velocities in Fig. 2. Statistically significant differences were found between the
children with CP in each test were statistically significant (each p- GGI of healthy children (Ref) and the GGIs of children with CP. The
value < 0.001). differences between unaffected and affected hemiplegic lower
limbs and affected diplegic limbs were confirmed by post hoc
3.2. Data analysis of clinical measurements analysis (each p-value <0.001).

The descriptive statistics for DROM I, DROM II and ASO for the 3.4. Correlation between GGI and DROM I, DROM II, ASO data
unaffected and affected lower limbs of children with spastic
hemiplegia and the affected lower limbs of children with spastic Table 3 summarises the correlation coefficients between
diplegia are presented in Table 2. Fig. 1 shows the effect of two clinical measures and GGI. The statistically significant correlations
different angular velocities, slow (V1) and fast (V3), on DROM, as are printed in bold and marked with an asterisk. There were only
measured in the four DAROM tests (T1–T4) of unaffected (n = 18; fair (0.21–0.40) and moderate (0.41–0.60) correlations.
1A) and affected (n = 18; 1B) lower limbs in children with
hemiplegia (HS) and the affected lower limbs of children with 4. Discussion
diplegia (DS; n = 36; 1C).
A main effect of the level of involvement was found in testing Spasticity is a common impairment that interferes with motor
the lower limbs of children with HS (F(1, 34) = 16.54 p < .001), function in children with CP.[12] The relationship between clinical
indicating that the average DROM of the affected leg was assessments of spasticity and gait analysis in patients with CP has

Table 2
Summary of clinical measurements (DROM I, DROM II, ASO) for unaffected (n = 18) and affected (n = 18) lower limbs in children with hemiplegia and affected (n = 36) lower
limbs in children with diplegia (as shown in Table 2). Normally distributed variables are summarised as the means and standard deviations, and non-normally distributed
variables are presented as the median and range. Non-parametric ANOVA test.

Hemiplegia Diplegia
Unaffected Affected Affected
Tests DROM I (8) DROM II (8) ASO (8) DROM I (8) DROM II (8) ASO (8) DROM I (8) DROM II (8) ASO (8)

T1 49.9  12.4 51.1  11.5 0.1 < -2–16> 49.6  7.4 56.3  8.1 6.7  3.9 50.8 < 35.5–59.9> 59.3  6.3 9.9  5.4
T2 13.6 < 7–32.1> 15.3  6.3 0.8  2 15  4.5 17  4.5 1.6 < 0.2–6.5> 14.2  2.3 23.5  3.5 10.6 < 1.8–14>
T3 10  4.1 10.2  3.4 0.2  5.3 11.2  5.3 24.9  5.7 13.6  5.2 30.6  13.6 32.3 < 18.2–59.5> 5.2 < -16–46.8>
T4 4.2  2.1 8.2 < 0.1–17.3> 4.8 < -8.2–10.6> 5.1  1.3 16.9 < 9.1–19.9> 12.7 < 3.7–15.8> 2.5 < 0.4–7.8> 4.3 < -7.8–23.3> 1.5  7.1
M. Domagalska et al. / Gait & Posture 38 (2013) 1038–1043 1041

Fig. 1. The effects of the angular velocities (slow, V1, and fast, V3) applied in the DAROM tests (T1–T4) to measure the deficit of ROM (DROM) in the unaffected lower limbs of
children with HS hemiplegia (n = 18; 1A), the affected lower limbs of children with HS hemiplegia (n = 18; 1B) and the affected lower limbs of children with DS diplegia (n = 36; 1C).
The angle of spasticity (ASO) in the unaffected and affected hemiplegic lower limbs (1D), the affected lower limbs of children with hemiplegia (HS; n = 18) and the affected lower
limbs of children with diplegia (DS; n = 36; 1E) are shown. Nonparametric ANOVA tests were used for comparisons. Vertical lines indicate the levels of confidence.

been described in several studies. Damiano and Abel [21] reported findings are in agreement with Kerrigan et al. [24], who also
a significant correlation between the knee extensor Ashworth reported other causes of a stiff knee gait, including impaired
score and gait impairment. Spasticity of the rectus femoris was dynamic hip flexion and poor ankle mechanics.
reported as the primary cause of a stiff knee gait.[22,23] These The results of this study show that deviations from normal gait
in patients with CP generally do not depend on the static and/or
dynamic contractures of hip and knee flexors. Although the GGI
detected statistically significant correlations for a few clinical
measures, the majority of correlation coefficients were low. Our

Table 3
Correlation coefficients. Statistically significant correlations between clinical and
GGI scores are indicated in bold.

Tests Spearman’s R p-Level

T1 GGI & DROM I 0.053 0.6590


GGI & DROM II 0.131 0.2741
GGI & ASO 0.216 0.0687
T2 GGI & DROM I 0.054 0.6519
GGI & DROM II 0.158 0.1837
GGI & ASO 0.493 0.0006
T3 GGI & DROM I 0.481 0.0000
GGI & DROM II 0.381 0.0009
GGI & ASO 0.143 0.2323
T4 GGI & DROM I 0.234 0.0481
GGI & DROM II 0.269 0.0223
GGI & ASO 0.209 0.0783
Fig. 2. The effect of lower limb involvement level on GGI.
1042 M. Domagalska et al. / Gait & Posture 38 (2013) 1038–1043

results were consistent with those reported by Orendurff et al. [25] children with CP. However, the weak relationship between clinical
and McMulkin et al. [26], who found only weak correlations examination and the index for quantifying deviations from normal
between gait analysis and clinical examination measures, includ- gait does not indicate the superiority of either method. Rather, it
ing ROM, in children with CP. Desloovere et al. [27] also explored indicates their complementary nature. Moreover, clinical exami-
the relationship between gait analysis and clinical examination nation focuses on the primary abnormalities of children with CP,
parameters. She found poor correlations between spasticity of the which arise directly from the damage to the CNS (e.g., abnormal
hip flexors and adductors, the hamstrings, the rectus femoris, the muscle tone, abnormal reflex activity, loss of selective muscle
gastrocnemius, and gait parameters. control, spasticity) and from secondary effects (contracture and
Our results, which found the highest correlation between GGI deformations), resulting from abnormal bone and muscle growth.
scores and rectus femoris spasticity, are consistent with the results The pathological gait is characterised not only by primary and
presented by Desloovere et al., who reported fair to moderate secondary problems but also by compensatory mechanisms
correlations between rectus femoris scores (assessed using MAS (tertiary effects). The lack of correlation between the two
and MTS) and gait data [27]. Desloovere et al. evaluated spasticity measurements supports the view that both data sets are critical
using MA and MT scores and investigated these scores’ dependence for interpretation and treatment decision-making in children with
on separate gait kinematic parameters; in contrast, our study was CP. A shortcoming of this study was the spasticity measurement in
based on the DAROM method, objective accelerometric measure- the proximal muscles of the lower extremities. In many CP
ments and a global index for quantifying deviations from normal children, distal muscles are more severely affected, and this is
gait. In children with CP, spasticity is commonly assessed with the especially true of hemiplegic children. In future work, the
MTS, using goniometric measurements of ROM while applying spasticity assessment of the calf muscles will be added to
three different velocities [3,28,29]. Many authors report that the investigate the association between the DAROM of all lower limb
MTS correlates poorly with the degree and type of muscle tone muscles and their activity in the relative gait phase.
disorders in children with CP because of a strong relationship
between ROM and adjacent joint position.[2,8,28] Additionally, Conflict of interest statement
goniometric measurements do not allow for simultaneously
measuring the applied velocity of passive movement and The authors declare that they have no conflict of interest.
corresponding ROM.
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