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Lee 2008

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Disability and Rehabilitation, 2008; 30(19): 1439–1444

RESEARCH PAPER

Therapeutic effects of strengthening exercise on gait function of


cerebral palsy

JUNG HWAN LEE, IN YOUNG SUNG & JONG YOON YOO

Department of Physical Medicine and Rehabilitation, Asan Medical Center, Ulsan University College of Medicine, Seoul,
Korea
Disabil Rehabil Downloaded from informahealthcare.com by Selcuk Universitesi on 01/17/15

Accepted August 2007

Abstract
Purpose. To assess the effectiveness of strengthening exercises of the lower limbs on improvement of muscle strength and
gait function.
Method. Those included were diagnosed as spastic diplegic or hemiplegic type of cerebral palsy (CP) and verified as grade 2
or 3 of the Gross Motor Function Classification System (GMFCS). Participants were divided into an experimental group
(n ¼ 9) or a control group (n ¼ 8). The experimental group completed a 5-week strengthening program and the control group
For personal use only.

took part in conventional physical therapy. Muscle tone and strength of lower limb, Gross Motor Function Measure, lateral
step up, squat to stand, and three dimensional gait analysis were tested at pre-training, post-training, and 6 week follow up.
Results. Maximal hip extensor strength, and number of squat to stand were significantly increased at post-training and
6 weeks follow up in the experimental group compared with the control group. GMFM score D and E significantly improved
in the experimental group at post-training. The experimental group demonstrated significant increase of gait speed and stride
length and decrease of double support phase at post-training and 6 weeks follow up.
Conclusions. Strengthening exercises could be a useful method to improve gait function of patients with spastic CP.

Keywords: Cerebral palsy, strengthening exercises, gait analysis

evidence of increase of spasticity or abnormal move-


Introduction
ment [1 – 6]. Despite many reports reporting the
Muscle weakness, impairment of control over muscle positive effects of strengthening exercises, there were
tone, posture, and performance are major factors few randomized controlled trials so that it was
contributing to various physical dysfunctions in difficult to evaluate the benefits of this program
cerebral palsy (CP). Neurodevelopmental or Bobath compared to conventional physical therapy. Also,
therapy has long cautioned against strengthening there were few reports that evaluated the effects of
exercise, with the assumption that the effort involved this program by three dimensional gait analysis or
would increase spasticity, co-contraction, associated other sophisticated methods measuring gait function.
reactions and abnormal movement patterns. These Thus, the objectives of this study were to determine
therapies mainly concentrate on control over muscle whether strengthening exercises of the lower extre-
tone or reflex that was abnormally manifested. But mities could increase the strength of the lower limb
increasing number of studies have reported that muscles and improve walking ability in children with
strength-training programs can improve muscle cerebral palsy by physical and functional evaluation
strength and the performance of activities such as as well as quantitative three dimensional gait
walking in patients with cerebral palsy with no analysis.

Correspondence: In Young Sung, MD, PhD, Department of Physical Medicine and Rehabilitation, Asan Medical Center, Ulsan University College of
Medicine, 388-1 Pungnap-2dong, Songpa-gu, Seoul, 138-736, Korea. Tel: þ82 2 3010 3800. Fax: þ82 2 3010 6964. E-mail: [email protected]
The material in this paper was presented at a peer review poster presentation in the Annual Assembly of APMR in 2006, Honolulu, Hawaii.
ISSN 0963-8288 print/ISSN 1464-5165 online ª 2008 Informa UK Ltd.
DOI: 10.1080/09638280701618943
1440 J. H. Lee et al.

Methods Patients of the control group took part in conven-


tional physical therapy including NDT, range of
Study population
motion exercise, and gait training for 5 weeks.
Potential participants aged between 4 and 12 years All patients undertook physical examination such
old were recruited from the outpatients’ clinic of our as tone and strength of major muscle groups of lower
Department of Physical Medicine & Rehabilitation. limb, functional test estimated by the Gross Motor
Those included were diagnosed as spastic diplegic or Function Measure (GMFM) and number of lateral
hemiplegic type of CP and could ambulate with or step up and squat to stand they could do during 30
without assistive devices or orthosis, therefore, minutes, and three-dimensional gait analysis as a
verified as grade 2 or 3 of the Gross Motor Function baseline measurement before beginning the thera-
Classification System (GMFCS). They were ex- peutic sessions. Muscle strength and tone was
cluded from the study if they were not able to follow measured only on the hemiplegic side in hemiplegic
commands from therapists, had fixed contracture at types and bilateral sides in diplegic types, by the
the knee or hip joint of more than 25 degrees, had same physician. Muscle tone was assessed by testing
medical or orthopedic diseases that prevented them the resistance to passive stretch using a Modified
Disabil Rehabil Downloaded from informahealthcare.com by Selcuk Universitesi on 01/17/15

from exercising, or had received orthopedic surgery Ashworth Scale (MAS) and muscle strength was
of the lower limb or injection of an antispastic drug evaluated by testing overall strength of major muscle
(e.g., phenol injection, botulinum toxin injection). groups using the Manual Muscle Test (MMT),
Children and parents who gave informed consent to which were graded from 0 to 5. The GMFM is a
this study were selected and 16 patients were validated instrument designed to assess motor status
recruited. Ethics approval was obtained from the in CP and to quantify change over time or as a result
Institutes of Review Board (IRB). Participants were of intervention. It consists of 88 items within five
allocated randomly to either the experimental group dimensions that span the range of activities that most
(n ¼ 9) or control group (n ¼ 8) using concealed individuals encounter in their daily activities: (A)
methods. No significant difference was found in lying and rolling, (B) sitting, (C) crawling and
For personal use only.

distribution of age, sex and, type of spastic CP kneeling, (D) standing, and (E) walking, running,
between the two groups (Table I). and jumping. Scores are expressed as a percentage so
that a normally developing 5-year-old child would be
100%. And separate scores can be calculated for
Procedures
each of the five dimensions as well as a total score
Patients in the experimental group completed a 5- [7]. Participants in this study could ambulate with or
week strengthening program targeting the muscle without assistive devices or orthosis, therefore,
groups of lower limbs. The frequency of the sessions Dimension D, E score, and total score were
was three times per week and the duration of each measured. GMFM, lateral step up, and squat to
session was 60 minutes. It consisted of warm up stand were evaluated by the same physical therapist.
stretching exercise, squat to stand, lateral step up, Computerized gait analysis, including linear para-
stair walk up and down, isotonic exercise of lower meter, kinematics, and kinetics at freely selected
limb muscles, isokinetic exercise utilizing a bicycle, speeds was performed using Orthotrak 6.2.4 sys-
and a cool down exercise. For isotonic exercise, one tem1 (MotionAnalysis, USA). The linear para-
of three weights, 0.25 kg, 0.45 kg or 0.9 kg, was meters included walking velocity, cadence, stride
selected to provide resistance to voluntary muscle length, and percentage of single and double limb
contraction in the form of adjustable weight cuffs support. For the gait analysis passive markers were
attached by Velcro straps to the subject. Each patient attached with adhesive tape on following location of
performed in 2 sets of 10 repetitions in each muscle both lower limbs: the anterior superior iliac spines,
group. Selected weight was determined by the sacrum, anterior aspect of the midthigh, the knee and
physical therapist depending on the ability of the the midcalf, the lateral malleolus, the base of heel,
children completing 2 sets of 10 repetitions. and the dorsum of foot between second and third
metatarsals. The child was asked to walk indepen-
dently if possible, but was allowed to use an assistive
Table I. General characteristics of experimental and control group. device if necessary. After completing 5 weeks of three
sessions, all patients were verified by the same
Experimental Control
measurements mentioned above to investigate effects
Age (years) 6.3 + 2.1 6.3 + 2.9 of strengthening exercise compared to conventional
M:F 4:5 6:2 physiotherapy. Six weeks later, the same measure-
Type ments were also conducted in both groups to find
Diplegia 4 5
out whether the effects of the strengthening exercises
Hemiplegia 5 3
could persist for 6 weeks after finishing the therapy.
Strengthening exercises in cerebral palsy patients 1441

not significantly changed in all patients of the


Data analysis
experimental and control groups.
Measured muscle strength was graded from 0 to 5 in
each muscle group and the strength of each muscle
Functional tests at pre- and post-strengthening exercise,
group was compared between the two groups.
and 6 weeks follow up
Kinematic and kinetic parameters were obtained in
hemiplegic limb in hemiplegic type and bilateral The number of lateral step ups during 30 minutes
limbs in diplegic type and each parameter of was increased after training and 6 weeks follow up in
kinematic, kinetic, and linear parameters was com- both groups and the experimental group showed a
pared between two groups. SPSS version 12.0 was greater increase than the control group but not to a
used to analyze the data and level of significance was significant degree. Number of squat to stand was
set at 5%. A repeated measures parameter ANOVA significantly increased in experimental group com-
design, with time as the main factor allowed the pared with control group, which persisted at 6 weeks
comparison of means between two groups at three follow up. GMFM score D and E significantly
measurement times (baseline, post-training, six week improved in experimental group, but improvement
Disabil Rehabil Downloaded from informahealthcare.com by Selcuk Universitesi on 01/17/15

follow up). disappeared at 6 weeks after cessation of training.


There was no significant change in total GMFM
score in experimental group in comparison with
Results control group (Table III).
Muscle strength at pre- and post-strengthening exercise,
and 6 weeks follow up Data of gait analysis for the sagittal plane at pre- and
post-treadmill training
Maximal hip extensor strength was significantly
increased at post-training and was better maintained The experimental group demonstrated a significant
at 6 weeks follow up in the experimental group increase of gait speed and stride length compared
For personal use only.

compared with the control group. The strength of with control group at post-training and 6 weeks
other muscle groups did not show significant follow up. There was a trend of increased percent of
improvement following strength training in the single limb support without statistical significance
experimental group (Table II). Muscle tone was and significant decrease in the percent of double

Table II. Muscle strength at pre- and post-strengthening exercise, and 6 weeks follow up.

Pre training Post training Follow up at 6 weeks

Experimental Control Experimental Control Experimental Control

MPHflex 3.4 + 0.7 3.5 + 0.5 3.7 + 0.5 3.5 + 0.5 3.8 + 0.4 3.5 + 0.5
MPHabd 3.2 + 0.7 3.3 + 0.7 3.6 + 0.5 3.3 + 0.7 3.6 + 0.5 3.3 + 0.7
MPHext 3.0 + 0.7 2.9 + 0.9 3.3 + 0.7 2.9 + 1.0* 3.4 + 0.7 2.9 + 1.0*
MPHaddj 3.1 + 0.8 3.0 + 0.7 3.2 + 0.6 3.0 + 0.7 3.4 + 0.7 3.0 + 0.8
MPKflex 3.2 + 0.5 3.3 + 0.7 3.4 + 0.7 3.3 + 0.7 3.4 + 0.8 3.3 + 0.7
MPKext 3.4 + 0.5 3.6 + 0.5 3.7 + 0.5 3.6 + 0.5 3.7 + 0.5 3.6 + 0.5

Values are mean + standard deviation (*p 5 0.05). MPHflex, muscle power of hip flexor; MPHabd, muscle power of hip abductor;
MPHext, muscle power of hip extensor; j MPHadd, muscle power of hip adductor; MPKflex, muscle power of knee flexor; MPKext, muscle
power of knee extensor.

Table III. Functional tests at pre- and post-strengthening exercise, and 6 weeks follow up.

Pre training Post training Follow up at 6 weeks

Experimental Control Experimental Control Experimental Control

Lateral step up 6.4 + 4.1 6.6 + 4.7 9.3 + 4.8 8.5 + 4.7 9.5 + 5.3 8.3 + 5.2
Squat to stand 11.6 + 6 13.8 + 5.6 13.2 + 5.4 14.1 + 5.8* 13.7 + 5.9 14.4 + 5.9*
GMFMT 86.5 + 13.3 85.2 + 13.4 86.9 + 13.4 85.4 + 13.5 87 + 13.5 85.7 + 13.3
GMFMD 73.5 + 25.7 74.5 + 23.7 73.7 + 26.6 74.6 + 23.7* 73.8 + 26.6 75.4 + 22.7
GMFME 61.6 + 34.1 61.4 + 33.9 62.7 + 34.1 61.4 + 33.9* 63.0 + 34.4 61.8 + 34

Values are mean + standard deviation (*p 5 0.05). GMFMT, total score of Gross Motor Function Measure; GMFMD, score of category D
of Gross Motor Function Measure; GMFME, score of category E of Gross Motor Function Measure.
1442 J. H. Lee et al.

limb support in the experimental group (Table IV). Discussion


Maximal hip flexion was improved significantly in
experimental group in kinematic data at post-training Strength is an important aspect of normal motor
(Table V). In kinetic data, maximal moment of hip control that is deficient in patients with CP as well as
flexor was found to be improved after cessation of other upper motor neuron diseases. This study has
training but this improvement was not maintained profound meaning in providing evidence that a
after 6 weeks follow up (Table VI). strengthening program had positive influences on

Table IV. Linear parameters at pre- and post-strengthening exercise, and 6 weeks follow up.

Pre training Post training Follow up at 6 weeks

Experimental Control Experimental Control Experimental Control

Speed (cm/s) 54.7 + 30.7 69.8 + 43.0 74.6 + 38.7 68.2 + 42.9* 78.2 + 39.3 67.8 + 37.2*
Stride length (cm) 62.5 + 21.8 70.0 + 32.1 80.0 + 26.4 68.3 + 24.6* 83.9 + 28.6 71.3 + 22.9*
Disabil Rehabil Downloaded from informahealthcare.com by Selcuk Universitesi on 01/17/15

Cadence 106.8 + 37.1 107.9 + 48.4 109.7 + 26 101.1 + 47.4 112.9 + 19.0 105.3 + 36.4
Single support (%) 35.8 + 10.0 38.2 + 9.2 39.3 + 11.0 36.5 + 12.1 38.1 + 11.0 36.2 + 7.3
Double support (%) 22.0 + 11.9 23.7 + 17.6 15.8 + 12.9 27.0 + 22.7* 18.1 + 12.9 27.6 + 14.1*

Values are mean + standard deviation (*p 5 0.05).

Table V. Kinematic parameters at pre- and post-strengthening exercise, and 6 weeks follow up.

Pre training Post training Follow up at 6 weeks


For personal use only.

Experimental Control Experimental Control Experimental Control

MaxHflex 57.3 + 7.2 57.7 + 4.4 60.5 + 4.1 53.4 + 5.0* 59.1 + 5.9 55.5 + 6.5
MaxKflex 59.0 + 9.6 65.4 + 6.1 64.6 + 9.4 64.6 + 5.6 62.7 + 10.5 64.5 + 4.9
MaxAPF 8.2 + 7.9 7.7 + 5.4 9.1 + 8.4 7.4 + 5.4 10.3 + 9.5 7.4 + 5.8
MaxPAT 30.3 + 6.4 25.3 + 3.7 31.5 + 6.8 23.5 + 5.6 30.1 + 8.4 24.3 + 5.9
MinHflexj 13.7 + 8.8 7.9 + 7.0 10.2 + 9.7 1.1 + 8.0 10.6 + 13.0 8.9 + 21.0
MinKflex 5.9 + 10.7 5.3 + 10.7 2.2 + 11.2 1.1 + 11.2 4.1 + 11.7 8.6 + 20.7
MinAPF 714.1 + 8.9 720.1 + 8.1 717.1 + 9.0 720.8 + 11.2 715.3 + 7.6 715.3 + 7.3
MinPAT** 20.7 + 4.2 18.2 + 4.1 22.3 + 4.4 15.4 + 3.0 21.5 + 8.1 18.4 + 6.4

MaxHflex, maximal angle of hip flexion; MaxKflex, maximal angle of knee flexion; MaxAPF, maximal angle of ankle plantarflexion;
MaxPAT, maximal angle of pelvic anterior tilt; j MinHflex, minimal angle of hip flexion; MinKflex, minimal angle of knee flexion; MinAPF,
minimal angle of ankle plantarflexion; MinPAT, minimal angle of pelvic anterior tilt.

Table VI. Kinetic parameters at pre- and post-strengthening exercise, and 6 weeks follow up.

Pre training Post training Follow up at 6 weeks

Experimental Control Experimental Control Experimental Control

MaxHflexM 0.9 + 0.6 0.8 + 0.6 0.9 + 0.5 0.9 + 0.6* 1.3 + 0.5 0.9 + 0.4
MaxKflexM 0.1 + 0.1 0.1 + 0.3 0.2 + 0.3 0.1 + 0.1 0.2 + 0.3 0.1 + 0.2
MaxAPFM 0.7 + 0.5 0.6 + 0.4 0.6 + 0.3 0.7 + 0.3 0.9 + 0.3 0.8 + 0.3
MinHflexM 70.3 + 0.1 70.2 + 0.1 70.3 + 0.3 70.2 + 0.1 70.2 + 0.1 70.1 + 0.2
MinKflexMj 70.5 + 0.3 70.4 + 0.2 70.4 + 0.2 70.5 + 0.3 70.6 + 0.3 70.4 + 0.3
MinAPFM 70.1 + 0 70.1 + 0.2 70.1 + 0.1 0.0 + 0.1 70.1 + 0.1 0.0 + 0.3
MaxHP 1.7 + 1.1 1.7 + 1.2 1.5 + 0.9 1.7 + 1.1 2.4 + 1.4 2.0 + 0.9
MaxKP 0.6 + 0.5 0.7 + 0.7 1.0 + 0.8 0.7 + 0.7 1.2 + 0.8 0.9 + 0.6
MaxAP 0.6 + 0.5 0.6 + 0.7 0.8 + 0.6 0.7 + 0.6 0.9 + 0.8 0.9 + 0.7
MinHP 70.5 + 0.7 70.4 + 0.3 70.6 + 0.8 70.4 + 0.4 70.6 + 0.4 70.1 + 0.4
MinKP 71.1 + 0.8 70.7 + 0.6 71.3 + 1.4 70.8 + 0.6 71.3 + 0.5 70.7 + 0.5
MinAP 71.0 + 0.9 70.7 + 0.4 70.7 + 0.6 70.9 + 0.6 71.2 + 0.8 70.8 + 1.0

Values are mean + standard deviation (*p 5 0.05). MaxHflexM, maximal moment of hip flexion; MaxKflexM, maximal moment of knee
flexion; MaxAPFM, maximal moment of ankle plantarflexion; MinHflexM, minimal moment of hip flexion; MinKflexM, minimal moment
of knee flexion; MinAPFM, minimal moment of ankle plantarflexion; MaxHP, maximal hip power; MaxKP, maximal knee power; Max AP,
maximal ankle power; Min HP, minimal hip power; Min KP, minimal knee power; Min AP, minimal ankle power.
Strengthening exercises in cerebral palsy patients 1443

functional aspect including ambulation, which has with spastic CP. As a result, walking velocity and
been the most important aspect related to indepen- cadence were significantly increased, but stride
dency of patients with CP. It was argued that muscle length was not increased. They suggested that stride
strength of people with spastic CP was not weak and length was not shown to be related to strength in
that the impaired performance of functional activities lower limbs because stride length was the biomecha-
commonly observed is primarily a result of spasticity. nical effect of limitation in passive and active motion
Also, increased efforts associated with strength caused by spasticity. But although spasticity was not
training would increase spasticity in people with changed through strengthening exercise, increase of
neurological disorders and would lead to increased stride length was found in this study. This result
joint contractures and decreased motor function suggests that stride length could be increased as a
[7 – 9]. But this view was not supported by the result of increased strength of lower limb muscles.
experience of physicians and the clinical literature. A Increased strength of hip extensor contributed to
strengthening program was effective in increasing increase of hip flexor movement at terminal stance,
muscle strength and functional activities, whereas it which resulted in increased angle of hip flexion at
did not increase spasticity or bring about any swing phase and at last increased stride length. Also,
Disabil Rehabil Downloaded from informahealthcare.com by Selcuk Universitesi on 01/17/15

significant adverse effects [10 – 12]. Also in this improved ipsilateral single limb support resulted
study, none showed increased spasticity or developed from strengthening hip girdle muscle might con-
abnormal posture all through the program and six tribute to larger contralateral limb progression.
week follow up periods in the group doing strength- The GMFM is a validated instrument designed to
ening exercises. Several participants complained of assess motor status in CP and consists of five
muscle soreness after the sessions, but it was dimensions [7]. Total score includes mobility status
transient and the degree of soreness was not too before acquiring ability of gait function. Instead, D
severe to interfere in maintaining this program. and E dimension focused mainly on ability related to
Many previous studies have examined the effect of gait function. Because participants of both groups
non-weight-bearing exercises with resistance pro- could ambulate with or without an assistive device,
For personal use only.

vided by free weights or isokinetic exercises (open the total score did not have significance. D and E
kinetic exercises) [3,4,6,12 – 14]. While Blundell score were significantly higher in the strengthening
et al’s study [15] conducted weight bearing exercises group than the conventional group, which was
(closed kinetic exercises) that were closely related to consistent with improvement revealed by three
functional activities including gait that involve the dimensional gait analysis. But this difference had
lower limbs. It is specificity of training that force and diminished 6 weeks later. Patients of strengthening
power generated by muscles is directly related to the exercise did not lose score 6 weeks later, instead, the
function being trained [16]. Task relevant training score of the conventional group increased to the level
has the potential to train specific muscle groups that was not different from the strengthening group.
required for specific task performances and is a very Conclusively, gait function that had been improved
important aspect of fulfilling functional improve- did not decrease at the time of the 6 week follow up.
ment. The purpose of this study was to find out the Not only were there immediate effects of strength
effectiveness of a strengthening program mainly on exercise, but the benefits of this program were
improvement of gait function rather than maximizing maintained for a period of six weeks after it had
muscle force production. Therefore, our study finished. Similar results were found in other reports
utilized weight bearing exercises such as lateral step [12,19]. The exact mechanism was not exactly
up, squat to stand, in addition to free weight isotonic known. Sharp et al. [19] suggested that prolonged
and isokinetic exercises. Apart from evidence of improvement might be secondary to subjects feeling
increased strength of hip extensor muscle estimated better about their physical abilities and leading more
by manual muscle test, functional status such as active lifestyles. Additionally, it was possible that
squat to stand, gait speed, and stride length was improved functional status resulted from muscle
found to be promoted, which might result from strengthening made the patients participate in more
specific training methods in close relation to func- independent activity and have more opportunity to
tional activities. conduct ambulation exercise efficiently. As a result,
In particular, increased muscle strength has been once a higher functional status is acquired, it would
shown to be highly related to gait function. There give the patients the ability to maintain and promote
were reports documenting its effects on gait function their function by themselves.
in adults recovering from strokes and more highly Apart from the improvements in muscle strength
related to functional status [17,18] and CP patients and functional status, another benefit was feeling of
[3,10,11]. Damiano et al. [3] assessed patients’ gait enjoyment, feeling of well-being or self-confidence
function utilizing three dimensional gait analysis to that this program might give children. The enjoy-
investigate effectiveness of strengthening training ment or feeling of competence was a very important
1444 J. H. Lee et al.

thing because it might improve the adherence and References


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