Comparison of short- and long-time action observation training (AOT) on upper limb function in children with cerebral palsy

Abstract

PURPOSE:

We compared short- and long-time action observation training (AOT) in terms of grip strength, the Quality of Upper Extremities Skills Test (QUEST), and the ABILHAND-Kids test.

METHODS:

In total, 10 children with cerebral palsy (CP) participated. The children were assigned randomly to experimental group (n = 5) and control group (n = 5). The experimental group observed video tasks of goal-directed action before performing tasks, for 30 minutes per day, three times per week, for 4 weeks. The control group observed and performed the same actions, 60 minutes per day, three times per week, for 4 weeks.

RESULTS:

Grip strength, QUEST, and ABILHAND-Kids test results improved significantly in both groups (p < 0.05). However, there was no significant difference between the experimental and control groups in any variable tested (p > 0.05).

CONCLUSION:

The 30 minutes AOT was as effective as 60 minutes AOT in improving grip strength and upper limb function in children with CP. The results of our study suggest that 30 minutes AOT is a simple and not very time-consuming therapy for improving upper limb function in children with CP. We recommend that 30 minutes AOT be used for treating upper limbs in the clinic and at home.

Keywords

Action observation cerebral palsy mirror neuron system upper limb function

1 Introduction

Cerebral palsy (CP) is a group of non-progressive and permanent movement disorders that causes restriction of activities in the foetal or newborn brain [1]. The movement deficits of CP frequently include poor coordination, muscle weakness, tremors, sensory deficits, and poor perception [2]. These clinical symptoms are associated with restricted motor skills and activities of daily living, such as reaching and grasping [3]. In unilateral CP, upper limbs are more commonly involved than the lower limbs [4]. In bilateral CP, lower limbs are more involved than upper limbs and upper limb function is clumsy [4]. For this reason, most children with CP often have difficulty in performing motor tasks with their both limbs [5].

Additionally, attention deficit is a common problem in children with CP [6]. Nakada [7] reported that some degree of cognitive impairment was also found in ∼97.7% of children with severe CP. Schenker et al. [8] found that ∼19% of children with CP have attention deficit-hyperactivity disorder (ADHD). Parkes and McCusker [9] suggested that ∼40% of children with CP have severe difficulties with concentration. Attention deficit of children with CP is one of the problems affecting motor learning. Therefore, in order to participate effectively in intervention, a simple, easy to understand, and preferably entertaining approach is required.

Conventionally, many therapeutic approaches have been used to improve upper limb function, including constraint-induced movement therapy (CIMT), hand-arm bimanual intensive therapy (HABIT), and intramuscular botulinum toxin A combined with therapeutic training. However, the concepts mentioned above involve rather intensive training and high numbers of repetitions, and their outcomes have been somewhat variable [10]. However, action observation training (AOT) has recently gained attention in improving upper limb function, not least because of its advantages, including simplicity, economy, and ease of use [11].

The mirror neuron system (MNS) is well defined as an exciting neuron that activates when the animal observe or execute meaningful hand movements by another [12]. In humans, the MNS has been found in the inferior frontal cortex and the inferior parietal cortex [12]. This knowledge of the MNS resulted in the development of AOT for upper limb function in humans. Sgandurra et al. [13] reported that AOT plus execution is more effective than execution alone in children with CP. Especially, the assisting hand assessment (AHA) scale and ABILHAND-Kids scores differed significantly between the experimental and control groups. Kirkpatrick et al. [14] also found that home-based AOT and repeated practice improved the function of the upper limb more than repeated practice alone in children with CP.

However, there is a dearth of supporting evidence on the effects of AOT on upper limb function in children with CP. Thus, the main purpose of this study was to compare short- and long-time AOT on upper limb function. We expected an improvement in upper limb function following AOT and that there would be no significant difference between short- and long-time AOT.

2 Methods

2.1 Participants

The experimental protocol for this study was approved by our institutional review board (2017-01-012-004). Prior to recruiting, a power analysis was performed using the G-Power software (ver. 3.1; University of Dusseldorf, Dusseldorf, Germany), based on the findings of a pilot study including five children. An ‘a priori’ power analysis with the Wilcoxon signed-rank test indicated that a sample size of at least 10 children would provide an effect size of 1.14, a probability of 0.05, and a statistical power of 80%. Because the target sample size was 10, we recruited 10 children (5 experimental group with a mean age, 10.2±1.3 years; mean height, 129.2±3.4 cm; mean weight, 29.1±5.4 kg and 5 control group with a mean age, 9.4±1.3 years; mean height, 129.5±10.8 cm; mean weight, 34.3±7.9 kg) from pediatric rehabilitation units in Gyeongsangbuk-do. Prior to starting the study, all parents or caregivers read the experimental process form and signed an informed consent form. Inclusion criteria were as follows: (1) aged between 6 and 15 years, (2) confirmed diagnosis of spastic unilateral or bilateral CP, (3) below grade 2 on the modified Ashworth scale, (4) between grade 4 and 8 on the house functional classification system (HFCS), and (5) ability to understand the assessor’s instructions. All enrolled children were given an identification number and then were randomly selected by random allocation software (Isfahan University of Medical Sciences, Isfahan, Iran). Therefore, the children were divided randomly into the experimental (30 minutes) or control (60 minutes) groups. Table 1 lists the anthropometric and clinical characteristics of the children.

Table 1
Anthropometric and clinical characteristics of the children (n = 10)

Characteristics Experimental group (n = 5) Control group (n = 5) U p

Basic demographics

Age (years) 10.2±1.3^c 9.4±1.3 7.500 0.310

Sex (boys:girls) 2 : 3 2 : 3

Height (cm) 129.2±3.4 129.5±10.8 11.000 0.841

Weight 29.1±5.4 34.3±7.9 7.500 0.310

HFCS^a 5.0±0.7 4.8±0.8 10.500 0.690

CP^b type

Unilateral CP 3 2

Bilateral CP 2 3

Characteristics	Experimental group (n = 5)	Control group (n = 5)	U	p
Basic demographics
Age (years)	10.2±1.3^c	9.4±1.3	7.500	0.310
Sex (boys:girls)	2 : 3	2 : 3
Height (cm)	129.2±3.4	129.5±10.8	11.000	0.841
Weight	29.1±5.4	34.3±7.9	7.500	0.310
HFCS^a	5.0±0.7	4.8±0.8	10.500	0.690
CP^b type
Unilateral CP	3	2
Bilateral CP	2	3

^aHFCS: house functional classification system. ^bCP: cerebral palsy. ^cMean±SD.

2.2 Interventions

The children participated in 12 training sessions of upper limb exercise, three times per week, for 4 weeks. Prior to action observation, children in the experimental group were asked to select one of the six uni-manual tasks and two of six bi-manual tasks. The children in the control group were required to choose two of the six uni-manual tasks and four of six bi-manual tasks. For action observation, all children were seated in an armchair, positioned 1 metre away from a monitor during the AOT sessions. A 19 inch monitor screen was placed on an adjustable table. The video clip for each task was shown for 3 minutes, which was edited to simultaneously show forward, sideward, and backward directions in one screen. Each treatment session consisted of three (1 uni-manual task, 2 bi-manual tasks, and 30 minutes) or six (2 uni-manual tasks, 4 bi-manual tasks, and 60 minutes) goal-directed movements of AOT: action observation, execution with therapist guidance, and repeated practice. First, the child observed a 3 minutes action observation then was asked to execute the observed task for 3 minutes using the same tool. A therapist with five years experience sat beside the side of the child to guide appropriate movement and provide verbal comments during execution. We provided a 1 minute rest between sessions. A therapist for interventions would be not blinded to group allocation. The tasks are shown in Table 2.

Table 2
Observed tasks for intervention

Uni-manual tasks Bi-manual tasks

Press a rubber stamp Open a bottle lid

Stack cups Fold towel

Drink water with a cup Open a box

Grab a pen Put candies in a box

Flip cards Put Buttons

Put rings on a stick Make holes using a punch in a paper

Uni-manual tasks	Bi-manual tasks
Press a rubber stamp	Open a bottle lid
Stack cups	Fold towel
Drink water with a cup	Open a box
Grab a pen	Put candies in a box
Flip cards	Put Buttons
Put rings on a stick	Make holes using a punch in a paper

2.3 Outcome measures

All children underwent the screening test (prior to the interventions, T0), and then completed pre-test (on 1 week, T1) and post-test (the end of the interventions, T2). The tests included grip strength, the Quality of Upper Extremity Skills Test (QUEST), and the ABILHAND-Kids test. For grip strength, Jarmar hand dynamometer (Patterson Medical, Warrenville, IL) was utilized and the mean value of three grip strength was used for data analysis. For QUEST, dissociated movements, grasping ability, weight-bearing, and protective extension were measured. Grip strength and QUEST were assessed by a trained physical therapist with ten years’ experience and the ABILHAND-Kids questionnaire was filled out by the parents at the same experimental assessment time. All outcome measures were blinded to the interventions.

2.4 Statistical analysis

The Wilcoxon signed-rank test was used to compare pre- and post-intervention outcomes (grip strength, QUEST, and ABILHAND-Kids scores) for each group. The Mann-Whitney U–8209;test was used to compare grip strength, QUEST, and ABILHAND-Kids scores between the experimental and control groups. All statistical analyses were performed using the PASW Statistics software (ver. 20; Norusis/SPSS Inc., Chicago, IL, USA). The level of statistical significance was set at α= 0.05.

3 Results

3.1 Grip strength

Grip strength at the follow-up evaluation was significantly higher, from 3.80±1.78 psi (pre-test) to 4.80±1.75 psi (post-test) in the 30 minutes training group (p = 0.039) and from 4.11±1.74 psi (pre-test) to 5.12±2.02 psi (post-test) in the 60 minutes group (p = 0.042). However, there was no significant difference between the 30 minutes (1.00±0.35 psi) and 60 minutes groups (1.01±0.59 psi) at the end of each intervention (p = 0.841) (Table 3).

Table 3
Differences of results between groups (n = 10)

Experimental group (n = 5) Control group (n = 5) U p

Pre-test Post-test Post-Pre Pre-test Post-test Post-Pre

Grip strength (psi) 3.80±1.78^b 4.80±1.75 1.00±0.35 4.11±1.74 5.12±2.02 1.01±0.59 11.50 0.841

QUEST^a (%) 68.85±7.57 77.63±6.44 8.77±4.38 64.99±6.10 72.31±3.59 7.31±4.57 10.00 0.690

ABILHAND-kid (logits) 1.61±0.41 2.32±0.73 0.70±0.39 1.46±0.38 2.11±0.52 0.65±0.15 12.50 1.000

	Experimental group (n = 5)	Control group (n = 5)	U	p
Grip strength (psi)	3.80±1.78^b	4.80±1.75	1.00±0.35	4.11±1.74	5.12±2.02	1.01±0.59	11.50	0.841
QUEST^a (%)	68.85±7.57	77.63±6.44	8.77±4.38	64.99±6.10	72.31±3.59	7.31±4.57	10.00	0.690
ABILHAND-kid (logits)	1.61±0.41	2.32±0.73	0.70±0.39	1.46±0.38	2.11±0.52	0.65±0.15	12.50	1.000

^aQUEST: quality of upper extremity skills test. ^bMean±SD.

3.2 Quality of Upper Extremity Skills Test (QUEST)

QUEST scores improved significantly, from 68.85±7.57% (pre-test) to 77.63±6.44% (post-test) in the 30 minutes (p = 0.043) and from 64.99±6.10% (pre-test) to 72.31±3.59% (post-test) in the 60 minutes groups (p = 0.043). However, there was no significant difference between the 30 minutes (8.77±4.38%) and 60 minutes groups (7.31±4.57%) at the end of the interventions (p = 0.690) (Table 3).

3.3 ABILHAND-Kids test

Within-group score improved significantly, from 1.61±0.41 logits (pre-test) to 2.32±0.73 logits (post-test) in the 30 minutes training group (p = 0.043) and from 1.46±0.38 logits (pre-test) to 2.11±0.52 logits (post-test) in the 60 minutes group (p = 0.043). However, there was no between-group difference in the 30 minutes (0.70±0.39 logits) or the 60 minutes group (0.65±0.15 logits; p = 1.000) (Table 3).

4 Discussion

In the present study, we compared short (30 minutes) and long (60 minutes) periods of AOT on grip strength, the QUEST, and the ABILHAND-Kids test in children with CP. To our knowledge, this is the first clinical report comparing 30 and 60 minutes of AOT on grip strength, the QUEST, and the ABILHAND-Kids test in children with CP.

Overall, our findings indicated that the 30 minutes AOT approach was as effective as the 60 minutes AOT approach in improving upper limb function and performance in daily life. In our study, grip strength analysis revealed that grip strength increased in both the 30 minutes (8.6%) and 60 minutes (20%) groups after AOT. However, there was no significant difference between the 30 minutes and 60 minutes groups (p = 0.841). These results are consistent with a previous study that reported an increase in grip strength following such training: grip strength was improved by ∼3.0 mmHg after 2 weeks CIMT in unilateral CP [15]. Similarly, Stearns et al. [16] found that grip strength was increased by 24% following 2 weeks of function-based CIMT in six children with CP; they also observed a significant positive correlation between grip strength and acquired upper limb function was observed (r = 0.62, p < 0.05). Arnoould et al. [17] reported a significant relationship between grip strength and hand impairment (r = 0.52, p = 0.001).

In the present study, QUEST scores also improved after both 30 minutes (12%) and 60 minutes (11%) of AOT. The ABILHAND-Kids test revealed improvements in both the 30 minutes (44%) and 60 minutes (44%) groups after AOT. However, there were no significant differences between the 30 minutes and 60 minutes groups in any of these results (all p > 0.05). Similarly, several studies have reported a significant improvement after AOT in children with CP [13, 18], stroke patients [19, 20], and Parkinson’s disease patients [21, 22]. In a recent randomised control study, Sgandurra et al. [13] compared the effects of action observation plus execution versus action alone on upper limb function in 24 children with unilateral CP. They found that Assisting Hand Assessment (AHA) scores and Melbourne assessment outcomes were improved, by∼42% and∼7%, respectively, following 8 weeks of AOT with execution. They also observed a significant increase in ABILHAND-Kids scores following AOT with execution. Similarly, Buccino et al. [18] observed the effects of AOT by comparing action practice after action observation and action practice alone in 15 children with CP. They found that the mean Melbourne Assessment score increased significantly, from 86.87% to 94.25% in the AOT group. However, in the control (action alone) group, the mean score was not significantly different. Franceschini et al. [19] reported that box and block test results were improved significantly, from 8.3EA to 14.5EA, after 4 weeks of AOT in stroke patients.

The effects of AOT on upper limb function may involve a neurological mechanism. Observation of actions and actual execution activate similar neural structures, such as the premotor and inferior parietal cortex, in human brain imaging studies [23]. Neurological phenomena associated with improved upper limb function may result from MNS activation after the application of the AOT. Clinically, functional motor recovery involves an understanding of task, imitation task, practice of task, and facilitation of motor memory. Therefore, AOT might be a useful tool to use as a home program prior to actual training to promote therapeutic effectiveness.

Some main limitations should be considered in further studies. First, the present study involved a small sample of children for generalization. However, a power analysis was performed based on the results of a pilot study. Further studies with larger sample sizes are needed so that the role of AOT can be assessed fully and generalized. Second, the four weeks intervention is too short for assessing improvement in physical performance, thus a careful interpretation should be needed. Third, the present report does not include follow-up evaluation data. Future studies should assess longer-term follow-up results, which are important because it is difficult to maintain obtained functional improvements over 24 weeks in children with CP [13].

Finally, the grip strength data at the follow-up evaluation was statistically improved compared to the baseline in experimental and control groups. However, our study could not determine the measurement error for grip strength. In future studies, standard error of measurement and minimum detectable change should be estimated.

5 Conclusions

We suggest that 30 minutes of AOT is as effective as 60 minutes in improving grip strength and upper limb function in children with CP (p > 0.05). The results of our study suggest that 30 minutes AOT is a simple and not very time-consuming therapy for improving upper limb function in children with CP. We recommend that 30 minutes AOT be used for treating upper limbs in the clinic and at home.

Conflict of interest

None to report.

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	Experimental group (n = 5)			Control group (n = 5)			U	p
	Pre-test	Post-test	Post-Pre	Pre-test	Post-test	Post-Pre
Grip strength (psi)	3.80±1.78^b	4.80±1.75	1.00±0.35	4.11±1.74	5.12±2.02	1.01±0.59	11.50	0.841
QUEST^a (%)	68.85±7.57	77.63±6.44	8.77±4.38	64.99±6.10	72.31±3.59	7.31±4.57	10.00	0.690
ABILHAND-kid (logits)	1.61±0.41	2.32±0.73	0.70±0.39	1.46±0.38	2.11±0.52	0.65±0.15	12.50	1.000