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Abstract

OBJECTIVES:

To study the effect of induced fatigue of the unaffected limb on the sensory components of standing balance; proprioception and vestibular symptoms in children with hemiplegic cerebral palsy.

METHODS:

Setting: Outpatient Clinic of Faculty of Physical Therapy, Cairo University. Patients: Twenty-nine children with hemiplegic cerebral palsy [(ages 8.9 $\pm$ 2.3 years), motor ability I/II according to the GMFCS and spasticity of I/I $+$ according to the Modified Ashworth Scale]. Outcome Measures: Before and after the induced fatigue of the unaffected limb, the following measures were recorded: postural balance, using the Biodex Balance System and the Timed Up and Go test; vestibular sense, using the Paediatric Vestibular Symptom Questionnaire; and proprioception measures of both knees, using the Biodex isokinetic dynamometer.

RESULTS:

There was a significant increase in the post-fatigue values for the overall stability index ( $p<$ 0.05), the Timed Up and Go test ( $p<$ 0.05), reposition errors of proprioception of the unaffected limb ( $p<$ 0.05) and the vestibular questionnaire ( $p<$ 0.05); there was a non-significant decrease in the post-fatigue values for reposition errors of proprioception of the affected limb ( $p=$ 0.859).

CONCLUSION:

Fatigue of the unaffected limb negatively affects postural balance and related sensory systems (proprioception of the fatigued limb and vestibular function) but does not have an impact on proprioception of the unfatigued limb.

Keywords

Fatigue postural balance proprioception vestibular sense hemiplegic cerebral palsy

1. Introduction

Spastic cerebral palsy (CP) is a type of disability induced by a non-progressive lesion in one or more areas of the immature brain that interferes with development, including motion and posture [1]. This disorder is the major cause of motor impairment in children and has a prevalence of approximately 2 out of 1000 live births globally [2]. Hemiplegia, or one-sided weakness and spasticity caused by a lesion of the contralateral brain hemisphere, affects approximately 33% of the population of children with CP [3]. Most children with hemiplegia are at a level I or II on the Gross Motor Function Classification System (GMFCS) as they can typically walk without any assistive devices [4].

Many functional skills depend on appropriate balance control to help children recover from unexpected balance disturbances [5]. Children with CP require additional time to regain stability and present a greater excursion of their center of pressure (CoP) when restoring their balance on an unstable platform compared to typically developing (TD) children [6].

Balance is a perceptual-motor process that incorporates senses of position and movement based on feedback from the sensory processing of visual, proprioception and vestibular systems with motor responses to bring the body into equilibrium [7].

Fatigue is an important limiting factor in patients with spastic CP [8]; it may be related to changes or declines in physical function such as walking. Fatigue is described as being unable to keepa level of power output during or after a repeated muscle contraction [9, 10]. Fatigue disturbed motor control leads to the co-contraction of muscles during movement attempts, which affects proprioception [11].

Vision plays an important role in the successful execution of goal-directed activities [12]. Children with CP mainly use their visual sense to compensate for musculoskeletal and neuromotor deficits during postural stability activities [13].

The impact of fatigue on balance was previously examined in studies by Hart et al. [14] and Vitiello et al. [8]. They assessed the effect of fatigue on postural control in children with neuromuscular disease and hemiplegic CP respectively. They reported limitations of postural control after fatigue might be attributed to decrease in torque of the lower extremity joints; this decrease was caused by muscular weakness or by deficits of the muscle spindles which control proprioceptive capacities.

However, to the best of our knowledge, no studies have investigated the effect of local muscle fatigue on sensory systems of balance. Because children with hemiplegic CP have an asymmetrical pattern of weight-bearing, they bear their weight mostly on the non-paretic leg to compensate for muscle weakness in the paretic leg [15]. This asymmetric alignment (and spasticity) may cause muscle atrophy, growth retardation and weakness on the affected side, and negatively affect balance [15]. Therefore, the aim of the present research is to explore if any of the sensory components of balance control (proprioception or vestibular senses) are immediately affected by inducing fatigue of the unaffected limb of children with hemiplegic CP.

2. Materials and methods

This pre-test – post-test study was consistent with the ethical standards of the Helsinki Declaration. Research Ethics Committee’s approval of the Faculty of Physical Therapy, Cairo University was obtained prior to the data collection.

2.1 Participants

Based on a previous study by Hart et al. [14] and considering standing balance as our primary outcome, 29 participants were needed to detect a difference of 103 $\pm$ 190 mm (effect size $d=$ 0.42) with 80% power and an $\alpha$ level of 0.05.

Children with hemiplegic CP [20 boys and 9 girls (6–15 years)] were recruited from the Outpatient Clinic of Faculty of Physical Therapy, Cairo University. The inclusion criteria were a gross motor ability level of I/II according to the GMFCS and spasticity of I/I $+$ according to the Modified Ashworth Scale.

In order to test the effect of fatigue on only two of the sensory systems known to control postural balance, namely proprioception and vestibular senses, vision and visual perceptual sensation was ensured to be normal for all included children. Star cancellation test was used to exclude children with visuospatial neglect, which is the common visual problem in children with hemiplegic CP [16]. The test requires an A4 sheet representing different-size stars (40 stars with a size of 1.2 cm and 52 stars with 0.6 cm) distributed equally on the sheet’s right and left sides, and each child is requested to select the tiny stars. The relative difference is calculated through the following equation [(total stars on the right side-total on the left)/total number of marked stars]. Values greater than 0.08 are indicative to relative visuospatial neglect [17]. Children were also excluded if they had any orthopedic surgery or botulinum toxin injections within 12 months before the start of the study.

2.2 Assessment procedures

Assessments of balance, vestibular function, and proprioception for both knees were performed before and immediately after the induced fatigue protocol by the same assessor.

2.3 Balance assessment

To assess the effect of induced fatigue on standing balance control, both the Biodex Balance System and the Timed Up and Go test were administered before and immediately after the fatigue induction protocol.

2.3.1 Biodex balance system

The Biodex Balance System is an unstable tilting platform that permits objective assessment of the abilities of the participant to regulate standing postural stances. It measures the Overall Stability Index (OSI), anterior/posterior stability index (APSI) and medial/lateral stability index (MLSI). In addition, the Biodex Balance System is a reliable balance tool. Its Intra class Correlation Coefficient (ICC) reliability is $R=$ 0.92 (OSI), $R=$ 0.89 (APSI), and $R=$ 0.93 (MLSI) [18]. Each participant was asked to assume double-limb postural stances barefoot on the balance platform with their eyes open and to remain as stable as possible for 20 seconds [19]. All participants were tested at stability level 7 based on our preliminary pilot cases [20]. A high stability index is indicative of poor balance [21].

2.3.2 Timed Up and Go test

The Timed Up and Go test (TUG test) is a quick and valid tool for the assessment of functional mobility in the paediatric population [22]. The reliability of the TUG test is high, with Intra class Correlation Coefficients values between 0.834 and 0.996 [23]. The test was applied as follows: The child sat on an adjustable-height chair with feet flat on the floor and hips and knees at 90 ${}^{\circ}$ of flexion. Then, the child was asked to stand up, walk 3 meters as quickly as possible, turn around, walk back, and sit down on the same chair. Timing began when the test administrator said “Go” and stopped when the subject’s back touched the backrest of the chair. Shorter times on the TUG test indicate a better level of functional balance [22].

2.4 Sensory balance assessments

After ensuring that vision was within normal limits in the entire eligible sample by using the star cancellation test, this study focused on the effects of induced fatigue on the vestibular and proprioceptive senses controlling standing balance.

2.4.1 Evaluation of vestibular symptoms

The Paediatric Vestibular Symptom Questionnaire (PVSQ) is a valid and reliable measure used in children to identify and evaluate the severity of common vestibular symptoms. It includes eleven questions. Each item is rated 0 (never), 1 (almost never), 2 (sometimes), and 3 (most of the time); a “don’t know” category is also included. The total score ranges from 0–33, depending on the equation: total score/(total number of questions – “don’t know” replies) yields a score of 0–3, with high scores indicating greater symptom severity. The symptoms evaluated in the questionnaire include unsteadiness, feeling sick, pressure in the ear, blurred vision and headache [24].

2.4.2 Proprioception assessment

A Biodex system 3 Pro Isokinetic dynamometer (Biodex Medical, Inc., Shirley, NY, USA) was used to assess proprioception, intra class correlation coefficients for trial reliability (ICC 2, 1), and day-to-day reliability (ICC 2, k) [25]. The children were tested with closed eyes to decrease the use of visual cues related to the joint position. The subject’s leg was placed with the hips and a knee flexed at 90 ${}^{\circ}$ and was then moved to the target angle (45 ${}^{\circ}$ of knee flexion) by the examiner. Then, the subject was asked to move actively to reproduce the target joint angle. When the subject sensed that the leg was in the position of the target angle, the child pressed the hold switch to stop the dynamometer. Each child performed three trials, and the average of the trials was recorded [26].

2.5 Fatigue protocol

Fatigue protocol of the unaffected limb was induced using a Biodex system 3 Pro Isokinetic dynamometer (Biodex Medical, Inc., Shirley, NY, USA). The blindfolded subjects were seated in a comfortable semi-reclining position with the hip at a 70 ${}^{\circ}$ angle. Isokinetic fatigue protocol was applied using repetitions of 35 ${}^{\circ}$ reciprocal maximal concentric contractions of knee flexion and extension, with a range of motion of 90 ${}^{\circ}$ and an angular velocity of 60 ${}^{\circ}$ /s [27]. Fatigue point was reached when peak torque or work decreases to 50% of the maximum [28].

Assessments were performed in the following order before the fatigue protocol was introduced: postural balance assessment using the Biodex Balance System and TUG test, followed by vestibular system assessment using the PVSQ, and finally proprioception assessment (reposition error) of both knees using the isokinetic dynamometer. Following the fatigue protocol, we first assessed the proprioception of both knees. According to Hart et al. [14], a rest period of 10 min was allowed after the proprioception assessment to ensure fatigue recovery. Then, the induced fatigue protocol was repeated, followed by the immediate assessment of postural balance and vestibular sense. Before the main trial, the children were familiarized with the Biodex Balance System and the isokinetic dynamometer system. All tests were completed on the same day at the same physical therapy lab.

2.6 Statistical analysis

Data management and statistical analysis were performed using the Statistical Package for Social Sciences (SPSS) v. 21. Data were tested for normality using the Kolmogorov-Smirnov test and the Shapiro-Wilk test. Numerical data were summarized using means and standard deviations or medians and ranges. Categorical data were summarized as percentages. The paired $t$ -test was performed to assess the effect of induced fatigue of the unaffected limb on postural balance and related sensory systems (vestibular function and proprioception of both knees). All analyses were two-tailed. Pearson’s correlation was performed to assess the correlation between postural balance (stability index) and proprioception (reposition error). Spearman’s rho was used to assess the correlation between postural balance (stability index) and vestibular function (score of Paediatric Vestibular Symptom Questionnaire). $P$ -values $<$ 0.05 were considered significant.

3. Results

Twenty-nine children with hemiplegia participated in this study (20 boys and 9 girls). The means $\pm$ SD for age, weight, height, and body mass index (BMI) were 8.9 $\pm$ 2.3 years, 26.4 $\pm$ 7.8 kg, 123.3 $\pm$ 9.1 cm and 17.1 $\pm$ 2.9 kg/m ${}^{2}$ , respectively, Table 1.

Table 1
Demographic characteristics of the studied children

	Mean (SD)	Range
Age (years)	8.9 (2.3)	6–14
Weight (kg)	26.4 (7.8)	16–50
Height (cm)	123.3 (9.1)	113–153
BMI (kg/m ${}^{2}$ )	17.1 (2.9)	11.3–24.8
		Count %
Sex	Female	9	31
	Male	20	69
Affected side	Left	8	27.6
	Right	21	72.4
MAS	I	23	79.3
	I $+$	6	20.7
GMFCS	I	18	62.1
	II	11	37.9

SD: standard deviation; BMI: Body Mass Index; GMFCS: Gross Motor Function Classification System; MAS: Modified Ashworth Scale.

Table 2

Pre- and immediately post-induced fatigue comparisons of postural balance, the vestibular sense and proprioception (reposition error of both knees)

	Before		After		Mean	95% CI		Percent
	Mean	SD	Mean	SD	Difference	Lower	Upper	Change	$p$ value
Timed Up and Go test	8.2	1	8.6	1.1	0.4	0.3	0.5	5.3	$<$ 0.	001a
Overall SI	2.0	0.6	2.5	0.8	0.5	0.3	0.7	24.8	$<$ 0.	001a
AP SI	1.3	0.4	1.7	0.7	0.4	0.1	0.6	28.9	0.	003a
ML SI	1.5	0.6	1.9	0.7	0.4	0.1	0.6	23.9	0.	002a
Proprioception of affected limb	7.5	1.8	7.4	2.1	0.1	1.2	1	$-$ 1.2	0.	859a
Proprioception of unaffected limb	5.1	1.9	7.2	2.5	2.1	1.3	2.9	41.1	$<$ 0.	001a
PVSQ ${}^{*}$	0 (0–0.2)		0 (0–0.3)						0.	025b

a: paired t test; b: Wilcoxon signed rank test; PVSQ: Pediatric Vestibular Symptom Questionnaire; ${}^{*}$ : data presented as median and range. SI: stability index; AP: anteroposterior; ML: mediolateral.

There was a significant increase in the anteroposterior and mediolateral stability indices between the pre- and post-fatigue conditions, with $P$ values of $<$ 0.05 (Table 2). Additionally, there was a significant increase in the time taken for the TUG test ( $p<$ 0.05), reposition errors of proprioception of the unaffected limb ( $p<$ 0.05), and vestibular system questionnaire scores ( $p<$ 0.05). A non-significant decrease was only found when comparing the pre-fatigue and post-fatigue proprioception (reposition error) scores of the affected limb ( $p=$ 0.859). Post-fatigue, there was no correlation between proprioception of the affected limb with either the stability indices of the Biodex balance (overall, AP and ML stability indices), or postural balance based on the TUG test. No correlations were detected post fatigue between proprioception of the unaffected limb and postural balance (overall and ML stability index) or proprioception of the unaffected limb and postural balance using the TUG test. Only weak positive correlations were found for the anteroposterior direction ( $r=$ 0.454). Regarding vestibular sense and Biodex standing balance, no correlation was found (Overall and ML direction) and there was only a weak positive correlation in the anteroposterior direction ( $r=$ 0.342) (Table 3).

Table 3

Post-fatigue correlation between balance and proprioception of both knees and the vestibular system

Balance	Proprioception (affected limb)		Proprioception (unaffected limb)		Vestibular system
	r	$p$ value	r	$p$ value	r	$p$ value
Overall SI	0.084	0.664	$-$ 0.039	0.841	$-$ 0.002	0.994
AP SI	$-$ 0.277	0.146	0.454	0.013	0.342	0.069
ML SI	$-$ 0.236	0.217	0.134	0.487	0.082	0.671
Timed Up and Go test	$-$ 0.217	0.258	$-$ 0.189	0.326	$-$ 0.155	0.421

SI: stability index; AP: anteroposterior; ML: mediolateral; r: Pearson correlation coefficient.

4. Discussion

The present study investigated the effect of induced fatigue of the unaffected limb on postural balance and its sensory systems (proprioception of the knee and vestibular sense) in children with hemiplegic CP. The results showed that the short-term effects of fatigue caused limitations of postural balance in both the frontal and sagittal planes along with limitations of vestibular and proprioception senses of the fatigued limb, although not in proprioception of the contralateral limb.

The significant increase in the stability indices following the induced fatigue revealing disturbance of balance could be attributed to: the slower conduction of afferent signal from the fatigued muscles leading to slower propagation of efferent signals to maintain standing balance [29]. Second, fatigue in children with CP could have a greater effect on balance due to the increased cognitive effort needed to maintain a standing position while introducing such additional mental load. The increase in postural instability may result from the conflict between two simultaneous tasks in resolving the allocation of executive attention. Christ et al. showed that children with CP had a deficiency in their ability to inhibit irrelevant stimuli in carrying out a task [30]. Third, muscle fatigue increases the muscle spindle discharge, which disrupts the afferent feedback input to the CNS and causes alterations in the proprioceptive properties of joints, with a negative effect on postural balance [31].

The sensory systems that control balance can be affected when the muscles that maintain balance are fatigued, thus inhibiting appropriate balance control [32]. In addition to ligaments relaxation, the desensitizing effect of fatigue on muscle spindle and Golgi tendon alters the proprioceptive properties of joints, which may affect balance and increases the risk of injury [33].

A significant increase in the reposition error scores of proprioception for the fatigued limbs after induced fatigue was reported. This finding is consistent with those of Gandevia [34], who reported that under fatigue conditions, cortico-motor neuronal cell firing rates decrease and motor-evoked potentials increase, suggesting inappropriate cortical output. The proprioception is mainly signalled by muscle spindle afferents and slowly adapting skin receptors [35]. Local muscle fatigue and pain receptors are stimulated by metabolic products of muscle contraction that have a direct effect on the discharge of muscle spindles. Fatigue also induces qualitative changes as the discriminative capacity in the ensemble of the muscle spindle afferent is decreased [36]. The result also agrees with Forestier et al. [37], who indicated that local muscle fatigue may alter joint awareness and may both directly and indirectly affect neuromuscular control. The direct effect is a decrease in expected learning of joint position sense, which indirectly leads to increased joint laxity and impaired joint kinaesthesia and position sense.

There was a significant increase in the vestibular questionnaire score after induced fatigue, which reflects impaired vestibular function. This could be attributed to the effect of fatigue on the vestibular system via vestibular-somatosensory interaction [38]. The previous finding is consistent with the finding of Majlesi et al. [39] and Nelson et al. [40]. They concluded that fatigue may impair central sensory integration which may lead to reduced upright postural control, resulting in dizziness or vertigo.

4.1 Limitations

There are some limitations to our study. First, the practice or learning effect of the knee proprioception assessment may have affected the results. Second, recovery after fatigue procedures is a common limitation for all fatigue experiments. Third, balance is a sophisticated process that requires the coordination of multiple systems and constant adjustment, which may have affected the correlation results. Fourth, there was no control population of healthy children of the same age for comparison. Fifth, the small sample size of the study makes it difficult to generalize the results. Finally, the limited reviews discussing the integration of vestibular senses with fatigue.

5. Conclusion

Fatigue of the unaffected limb negatively affects postural balance and its sensory systems (proprioception of fatigued limb and vestibular function) but does not have an impact on proprioception of the unfatigued limb in children with hemiplegic CP. Further randomized clinical trials are needed to study both the immediate and long-term effect of fatigue on sensory components of postural control.

6. Clinical message

In clinical practice, equal care should be given to both of the lower limbs of children with hemiplegic cerebral palsy during regular paediatric rehabilitation sessions. The unaffected limbs of hemiplegic children should also receive attention to compensate for the overload they experience. Integration of sensory system stimulation should be taken into consideration during paediatric rehabilitation sessions.

Footnotes

Conflict of interest

The authors report no conflict of interest.

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Immediate effect of induced fatigue of the unaffected limb on standing balance,proprioception and vestibular symptoms in children with hemiplegia