Alternative exercise methods for children with cerebral palsy: effects of virtual vs. traditional golf training

Abstract

Aim: Sport activities can increase the number of motor tasks performed by children with disabilities, helping to motivate these children to sustain life-long exercise. The aim of this study was to investigate the effects of virtual and traditional golf training on balance, muscle strength, lower extremity flexibility and aerobic endurance in children with cerebral palsy.

Methods: 19 children with unilateral cerebral palsy were divided into two groups, each of them received either virtual (n = 9) or traditional (n = 10) golf training, for over 12 weeks with three days of a 60-minute session/day. The effect of golf training was assessed with the Gross Motor Function Measure-88, the Modified Ashworth Scale and Lateral Step Up, Curl Up, Six-Minute Walk, Sit and Reach, Modified Thomas, and balance tests.

Results: Both training methods were associated with improved lower extremity flexibility and muscle strength, aerobic endurance and Gross Motor Function Measure-88 compared with the pre-training baseline values (p < 0.05). There was no difference found between virtual and traditional golf training groups except for balance and lateral step up tests (p > 0.05).

Conclusions: Both virtual and traditional golf training applied for 12 weeks on children with unilateral cerebral palsy improved lower extremity functions and physical performance. The use of virtual and traditional training as a complementary application to reduce motor problems in children with cerebral palsy could enhance the sustainability of this type of training because of its edutainment features. Virtual golf has an important advantage over traditional golf in that (a) the latter can be expensive and inaccessible for people with disabilities, and (b) making virtual golf a safer activity.

Introduction

Cerebral palsy (CP), a permanent disorder that affects the control of movement and posture, is caused by non-progressive disturbances to the developing fetal or infant brain (Rosenbaum et al., 2007). Neurological and motor problems that occur in CP include: muscle tone abnormalities, decreased muscle strength, loss of selective motor control, impairment of balance and coordination, contractures, and bony deformities (Papavasiliou, 2009). Due to these problems, individuals with CP need to participate in impairment-targeted rehabilitation programs (Tatar, 2010), which could be hard to maintain over the lifespan of the individual for various reasons, including lack of motivation and routine-based nature of activities. Therefore, multidimensional intervention models, such as task-oriented sport programs, which promote physical, social and self-engagement should be used to sustain habitual physical activity. Based on task-oriented exercise programs, pursued with selected participants for three months, it can be suggested that golf sports, either traditional or virtual, may improve motor functions in children with CP by ensuring the sustainability of the exercise with motivational features.

Sports are accepted as a complementary rehabilitation method improving both the physical performance and the quality of life in individuals with disabilities (Chawla, 1994, Tatar, 2010). Children with CP who participate in sports that include different motor abilities such as swimming/aquatic exercise (Dimitrijević et al., 2012, Lai et al., 2015), horseback riding/hippotherapy (Tseng et al., 2013, Whalen and Case-Smith, 2012), climbing (Christensen et al., 2017), skiing (Sterba, 2006) and yoga (Mak et al., 2020) programs showed improvement in motor functions. Increasing the number of sports that these children can participate in will help them to perform motor tasks suitable for their own physical ability (Di Russo et al., 2010) and to maintain life-long exercising. Golf is a lifetime physical activity played on an open-air course, performed either as a group or individually, and is self-motivating in terms of encouraging its players to exercise. The aim of the game is to hit the golf ball into a small hole in as few shots as possible to successfully fulfill the game with the best score. The player can use a variety of shots: swing and putting (Hume et al., 2005). The golf swing includes the movement of multiple joints and muscle groups (Lephart et al., 2007, Tsang and Hui-Chan, 2004). There are no studies that have been done to investigate the effect of traditional golf in CP. However, balance, proprioception, and mobility, all needed by children with CP, may be developed through golf training (Sell et al., 2007). Engaging individuals with disabilities in golf may also improve cardiovascular fitness, muscle strength and endurance, flexibility, speed and quality of movement (Shatil and Garland, 2000, Drane and Block 2006). While it has many advantages, in some types of CP, sudden and rapid golf swing movement may cause some reflexes to occur (asymmetrical and symmetrical tonic neck reflexes) and limit the participation of children with this condition. Assistive equipment may be needed when the subjects are non-ambulatory or do not have enough grip strength for holding the golf club. Transportation problems, access to golf courses and on-the-course golf mobility difficulties may not be resolved with adaptive technology or changes in game rules. In these situations, virtual reality interventions can help to overcome environmental barriers, providing an ecologically valid environment that is similar to the real world (Chen et al., 2018).

Virtual reality (VR) is an alternative application, which enables some of the same sport activities to be conducted in a sustainable and entertaining manner without the need for a large physical space or sports equipment. VR provides repetitive goal-oriented practices and has the flexibility of adjusting task difficulties, visual and/or auditory feedback, and the potential of social play and interaction (Chen et al., 2018). Repetition of tasks and variability of practice improves performance, enabling the nervous system to build new muscular synergies to accomplish the task goal (Rahlin et al., 2020, Chen et al., 2018). Purposeful movement promotes active participation by increasing the motivation of children with cerebral palsy. Exercise through virtual reality has been shown to have positive effects on the motor functions of children with CP when compared with conventional therapy (Weiss et al., 2014, Chen et al., 2018, Do et al., 2016).

To the best of our knowledge, there is no literature investigating only the effects of virtual golf training on children with CP. However, there are some studies that include golf training combined with a variety of other sport games such as boxing, canoeing, bowling, tennis, and baseball, etc. (Deutsch et al., 2008, Sharan et al., 2012, Pourazar et al., 2018, Do et al., 2016). In one of the studies, VR intervention program using golf and bowling games significantly improved reaction time in children with hemiplegic CP (Pourazar et al., 2018). It was proposed that VR should be incorporated into the rehabilitation process of CP as this may increase the probability of skill transfer. In a case report by Deutsch et al. (2008), it is shown that VR programs using a variety of sport games (golf, boxing, tennis, bowling and baseball) enhanced motor performance such as visual perceptual processing, postural control and functional mobility of a diplegic child. Likewise, Sharan et al. (2012) found that virtual sport games provide improvements in balance and manual ability. However, their conclusion to justify improving upper limb function was highly questionable. In another study, bilateral arm training based on virtual reality (golf, canoe, swordsmanship and cycling) has been shown to be effective for enhancing upper limb skills on the affected side, as well as bilateral coordination ability in children with hemiplegic CP (Do et al., 2016). This study shows that virtual reality is an appropriate intervention tool to enhance the physical performance of children with cerebral palsy. In the aforementioned studies, the small sample size or the relatively small number of training sessions (11-12 sessions) can be considered as limitations. Therefore, the long-term effects of VR exercise programs in children with cerebral palsy should be investigated further.

Based on the literature, it is evident that traditional or virtual sport programs have positive effects on children with CP. However, the effect of virtual and traditional golf training on children with CP has not been investigated. Specifically, despite the positive effects of golf training on postural control, proprioception, mobility, cardiovascular fitness, and muscle strength in healthy individuals, the possible effects on children with CP are unknown. The prolonged inactivity of children with CP leads to increases in spasticity and contracture; thus, if the positive effects of the virtual golf training can be determined, it can be suggested as an alternative home-based virtual exercise method. Therefore, the purpose of this study was to examine the effects of traditional or virtual golf training in overcoming problems such as spasticity, loss of muscle strength, and balance that limit the daily life of children with CP. Furthermore, the effects of three-month virtual and traditional golf training programs on motor functions of children with CP were also compared.

Materials and methods

Participants

In this study, a total of 19 spastic unilateral children with CP (14 males, 5 females) aged between 6-12 years with GMFCS level I & II were included (Table 1). All subjects were divided into two matching groups with similar gross motor skill levels, receiving either virtual golf training (n = 9) or traditional golf training (n = 10) (Table 1). Sample sizes were calculated with the one sample test of Wilcoxon signed rank for the Gross Motor Function Measure-88 (GMFM-88) to deduce the statistical power using G-power software. Pre-post scores of that parameter had a mean difference of approximately 1.60 (the difference between 95.79 and 97.39) and a standard deviation of 0.86, demonstrating that 9 participants were sufficient for the acquisition of results at a power value of 0.8 and a significance level of 0.95. Children with hemiplegic cerebral palsy who had no past experience either in golf or in virtual sports training were included in the study. All participants were examined by a physician to determine the correctness of the diagnosis and the suitability of the child for participating in golf training. Children with CP continued their routine physiotherapy program during the study. The study was conducted in accordance with the Helsinki Declaration. Prior to the conduction of this study, the local research ethics committee approval was obtained (16.03.2013-13).

Table 1.

Characteristics of the participants.

		Training Groups
		Virtual Golf		Traditional Golf
		Mean	SD	Mean	SD
Age (year)		8.22	1.71	8.50	2.50
Height (cm)		126.86	10.02	125.85	12.17
Body Weight (kg)		26.64	5.65	28.25	8.22
Gender	Males	7		7
	Females	2		3
GMFCS	Level I	3		3
	Level II	6		7
Effected Side	Right	4		8
	Left	5		2

Note: GMFCS = Gross Motor Function Classification System.

Participant inclusion criteria were that children had CP at GMFCS level one or two; age 6-12 years old; with sufficient hand function to hold the golf club; the ability to understand and follow the golf training program. Children were excluded if they had a surgical intervention or botulinum toxin injection within the last six months; a history of seizure; severe cognitive, auditory, visual, etc. problems that might affect the ability to follow physical activity and the lack of cooperation with the instructor during game and tests; absence from golf training for three consecutive days or six total days.

Procedure

The intervention program consisted of 12 weeks of golf training, scheduled for three days/week for 60 min/day. Participants of both groups were instructed on basic golf movements for two weeks and continued their own training program after the second week (Figure 1). It was necessary for children in the virtual golf group to be able to practice the correct golf swing during the virtual game. The one-unit training included periods of warm up (10 min), golf training (40 min, modified from Schempp and Mattson’s teaching methods (2005)), and cool down (10 min) (Schempp and Mattsson, 2005). Both virtual and traditional golf training programs (Table 2) were applied by a certified golf coach with ten years of experience.

Figure 1.

Flow diagram of the study.

Table 2.

Golf Training Program.

	1st Month	2nd Month	3rd Month
1st Week	Teaching grip, stance and ball position Full swing practice	Transferring the body weight to the target side during down swing and follow through Training of each part of the swing separately	Keeping left arm straight during the swing Hitting to the target Training of each part of the swing separately
2nd Week	Teaching aim and ball position Full swing practice	Keeping golf club parallel to the ground during take away Increasing the club head speed during down swing Balancing with staying on tiptoe on the trial foot at finish Consecutive golf shot practice	Short shots full swing training Hitting repeated golf shots
3rd Week	Repeated full swing training with drills	Throwing the club head during down swing Standing upright during the finish position Hitting consecutive three shots at each repetition	Long shots full swing training Hitting consecutive three shots at each repetition Hitting consecutive ten shots at each repetition Hitting a moving ball
4th Week	Training of each part of the swing separately (a)Back Swing (b)Down Swing (c)Follow through	Turning the chest to the trail side during back swing Keeping club head perpendicular to target at impact Turning the chest to the target side during follow through Hitting consecutive ten shots at each repetition	Hitting consecutive three shots at each repetition Hitting consecutive ten shots at each repetition Hitting a moving ball
Modifications that have been made for children with cerebral palsy during golf training: Effected side wrist joint range of motion limitations of the participants were taken into consideration in adjusting the grip positions. For example: if spasticity effects the wrist joint range of motion, the child was allowed to grip the golf club in partially pronate position. Back swing lengths were adjusted according to the effected side shoulder range of motion of the participants During backswing phase, effected side wrist position adjusted to stretch wrist flexor muscles with the weight of the golf club During downswing phase, sudden flexion of the effected side wrist was avoided in order to prevent the activation of the wrist flexor muscles. Straight forward reach of the effected side palm was requested. During the follow-through phase, sudden toe tip of the affected ankle was avoided in order to prevent the activation of the plantar flexion muscles. It is allowed after the swing movement was completed to improve balance. At the end of the follow-through phase, the finish was performed with elbow extended.

In traditional golf training, we used two different golf clubs (one with a normal and one with a large club face) and two different balls (a golf ball and a large plastic ball). Regardless of their dominant side, the participants were trained to play golf with their hemiplegic (affected) side in order to provide the same training effect on the affected side. Thus, the golf club was carried towards the affected side during the back swing. Golf practice in the children with unilateral CP required no adaptive equipment.

In virtual training, the Xbox 360 Kinect™ (Xbox 360, Microsoft, United States) game console was used. The Xbox360 Kinect™ works via infrared light sensors. The natural body movements were monitored three-dimensionally without any additional devices (Lange et al., 2011). Xbox360 Kinect™ has been reported to have sufficient sensitivity for use in many rehabilitation applications (Fernandez-Baena et al., 2012).

Measures

Various tests were used to assess the effect of the 12-week virtual and traditional golf training programs on children with unilateral cerebral palsy. Gross Motor Function Measure-88 , Modified Ashworth Scale, lateral step up, curl up, six-minute walk, sit and reach, Modified Thomas, and static balance tests were used for evaluation. GMFM-88 and spasticity tests were administered by the physiotherapist within the research group, as these tests must be conducted by an expert. All tests performed on each child were completed on two different days. Modified Ashworth and gross motor measurements were performed on the first day; balance, lateral step-up, curl-up, sit-and-reach, and Modified Thomas tests were completed on the second day. Testing order and break times between tests have been shown in Figure 2. Tests were done before and after 12 weeks of training for both groups.

Figure 2.

Experimental design.

Gross Motor Function Measure-88 has five dimensions: lying and rolling, sitting, crawling and kneeling, standing and walking, running and jumping (Alotaibi et al., 2014). Items were scored on zero to four point scales with higher scores indicate better capacity. Percentage scores of each dimension and combined total test scores were calculated.

The Modified Ashworth Scale (MAS) was used to evaluate the spasticity level before and after the intervention. The current definition of spasticity describes involuntary muscle hyperactivity in the presence of central paresis (Dressler et al., 2018). MAS is used to measure spasticity and performed manually to assess the resistance of muscle to passive stretching (Bohannon and Smith, 1987). Spasticity was measured on the hip internal rotator, hip flexor, hip adductor, quadriceps, hamstring, gastrocnemius, and soleus muscles. Gastrocnemius spasticity was measured in knee extension position and while soleus spasticity was measured in the knee flexion position. MAS was used to determine the possible negative effects of golf training on muscle spasticity, as it is shown that, sudden high speed movements may increase spasticity in CP (Van der Krogt et al., 2009).

Lower extremity functional strength was assessed with the Lateral Step-up Test (LST). Test-retest reliability was found high for LST in children with CP (Verschuren, 2008). Before the test, the participants were instructed to stand with the extremity being tested next to 21 cm step with their feet parallel. At the start of the test, the children were asked to raise their leg up and place it on the step by fully extending the hip and knee of the tested leg. One repetition was counted as the tested leg was placed on the floor again. The number of completed repetitions within 30 s was counted and scored. The right leg was tested first in all children regardless of their affected or non-affected side.

Abdominal muscular strength and endurance were assessed using modified curl up test as specified in the Brockport Fitness Test Manual. This test is suggested for children with mild physical impairments (Winnick and Short, 2014, Fragala‐Pinkham et al., 2008). Tatar (2018) also investigated the applicability of the modified curl up test in cerebral palsy and was found it to be applicable with a rate of 91%. In this test, the children were positioned supine on the floor, knees flexed, and feet on the ground. A measuring strip was placed on the floor in this position. Then, the children were instructed to flex their torso and reach to the measuring strip with their fingers. Participants completed one curl at every 3 s until they were exhausted, up to a maximum of 75 curls.

Six-minute walk test (6MWT) was performed based on the guidelines of the American Thoracic Society (Maher et al., 2008). It has demonstrated good to excellent reliability in children with CP (Thompson et al., 2008). The test is a standardized, self-paced submaximal walking test used as a measure of walking capacity and aerobic endurance. It was scored as the maximum distance that the person can walk in 6 min. The subjects were instructed to walk as far as possible in 6 min, at their own speed. The practice trial was not given because similar results were found between the tests with or without the practice trial (Van Loo et al., 2004). Standardized encouragement based upon the American Thoracic Society was provided during the walk at every minute by the tester walking behind the participant in order not to influence the child’s walking (Maher et al., 2008).

Sit-and-reach test was used to evaluate the flexibility of hamstring and lumbar extensor muscles. The children were asked to sit on the floor and keep their legs hip-wide. They placed their bare feet on the testing box. They kept both knees fully extended during the bilateral measurement (Winnick and Short, 2014). During the test, they were instructed to reach forward as far as they could with their fingers along with the measuring board and wait for at least one second. Children were asked to keep their shoulders parallel, as the arm reach may differ because of spasticity in children with CP. The measurements were repeated 3 times for each position and the best repetition was recorded for evaluation. Sit and reach test was suggested as an applicable test (Winnick and Short, 1991, Tatar, 2018) which was also used to evaluate physical fitness performance of children with cerebral palsy (García et al., 2016, Mak et al., 2018).

Modified Thomas Test was used to measure the flexibility of hip flexor muscles. The children were asked to lie supine on a stretcher and bring one leg toward their chest without lifting their torso. The test was scored as follows: 3 points were given if the contralateral leg (the tested leg) stays on the stretcher with no hip flexion (0 degrees) while the participant lifts the other leg. 2 points were given if the hip flexion was observed between 0 and 15 degrees. Between 15 and 30 degrees, a score of 1 point was given. If the hip flexion was above 30 degrees, no points were recorded (Winnick and Short, 2014).

Static balance was measured by using the TekScan MatScan® System force platform (model 3150, Boston, USA) with 2288 sensors (1.4 sensors/cm2) and a 100 Hz sampling frequency. Static balance was measured while the participants stood quietly on a force plate, which measured vertical ground reaction forces. Balance measurements were done at a rate of 30 samples per second. The area of the center of force (COF area; cm²) was evaluated. The tests were applied for 30 s each, with eyes open (EO) and eyes closed (EC).

Data analysis

Statistical analyses were performed using the SPSS version 22 software (SPSS, SPSS Inc, Chicago, IL, USA). To assess the normality of the distribution of all data, the Shapiro-Wilk test was implemented. Results showed that variables were not normally distributed. Therefore, within group changes and between group comparisons of the virtual and traditional golf groups were analyzed using nonparametric tests. Therefore, pre- and post-training changes within groups were analyzed using the Wilcoxon signed-rank test. The differences between groups were compared with the Mann-Whitney U test using the difference between the pre- and post- values. All statistical tests were two-sided, where a p value < 0.05 indicated statistical significance. Effect sizes were calculated using the equation r = Z/√N (r, effect size; Z, Z-value; N, the number of participants) as suggested for nonparametric variables (Field et al., 2012). The absolute value of the effect sizes was used as suggested by Cohen for the non-directional (two-tailed) tests. Effect size r = 0.10-0.30 is considered a small effect, 0.30-50 a medium effect, and >0.50 a large effect (Cohen, 1988).

Results

After twelve weeks of golf training, it was found that the GMFM-88 score within both traditional and virtual groups was significantly higher (p < 0.05). However, there was no significant difference between groups in GMFM-88 (p > 0.05) (Table 3). Although traditional golf training decreased gastrocnemius and soleus spasticity (p < 0.05), virtual golf training did not indicate any statistically significant changes in none of the measured muscles, i.e. hip internal rotator, hip flexor, hip adductor, quadriceps, hamstring, gastrocnemius, and soleus spasticity (p > 0.05) (Table 4). Within both training groups, the increase in sit-and-reach, lateral step-up, six min walk, and curl up test scores were statistically significant between pre- and post-tests (p < 0.05). However, between groups results did not indicate any statistically significant difference (p > 0.05), except for the affected side lateral step-up test and eyes-open balance test (COF area) (Table 3). While the center of force area decreased significantly in the virtual golf group compared to the traditional golf group, improvement in lateral step-up test score was significantly higher in the traditional golf group (p < 0.05) (Table 3). The traditional and virtual golf training did not significantly change the Modified Thomas test scores on neither the affected nor the non-affected sides (p > 0.05).

Table 3.

Comparison of the pre - post test and between groups results.

		Pre - Test		Post - Test		Within Groups		Between Groups
		Mean	SD	Mean	SD	p value	Effect size	p value	Effect size
GMFM-88 (score)
	Virtual Golf	95.79	2.16	97.39	1.30	0.011*	0.851	0.278	0.267
	Traditional Golf	93.75	4.53	95.83	4.13	0.005*	0.889
Lateral Step Up - AS (reps)
	Virtual Golf	10.9	4.0	13.1	5.1	0.006*	0.908	0.028*	0.518
	Traditional Golf	7.9	4.7	11.9	5.7	0.005*	0.890
Lateral Step Up - NAS (reps)
	Virtual Golf	10.4	3.5	13.0	4.7	0.007*	0.900	0.315	0.259
	Traditional Golf	8.1	4.5	11.5	5.9	0.005*	0.898
Curl Up (reps)
	Virtual Golf	15.1	9.8	23.3	13.9	0.008*	0.891	0.905	0.028
	Traditional Golf	23.2	16.6	30.3	19.5	0.007*	0.855
Sit and Reach (cm)
	Virtual Golf	21.5	4.9	24.2	5.0	0.007*	0.892	0.604	0.132
	Traditional Golf	26.1	6.6	28.0	5.8	0.012*	0.790
Modified Thomas – AS (score)
	Virtual Golf	1.0	0.9	1.3	0.7	0.157	0.471	0.897	0.053
	Traditional Golf	1.8	0.9	2.1	0.6	0.083	0.548
Modified Thomas – NAS (score)
	Virtual Golf	1.5	0.9	1.8	0.7	0.317	0.333	0.897	0.037
	Traditional Golf	2.0	1.2	2.3	0.8	0.180	0.424
6 min Walk (m)
	Virtual Golf	455.8	72.5	510.4	71.4	0.018*	0.789	0.536	0.158
	Traditional Golf	474.5	66.5	530.9	76.6	0.038*	0.656
Eyes Open-COF Area (cm2)
	Virtual Golf	2.9	2.0	1.2	0.9	0.026*	0.744	0.021*	0.530
	Traditional Golf	2.5	1.1	3.5	2.6	0.102	0.517
Eyes Closed-COF Area (cm2)
	Virtual Golf	1.9	0.9	2.0	1.7	0.891	0.046	0.633	0.122
	Traditional Golf	3.6	2.2	3.4	1.5	0.794	0.083

Notes: AS: Affected Side, NAS: Non-Affected Side, COF: Centre of Force, *for p < 0.05.

Table 4.

Comparison of the modified ashworth test scores of pre - post test and between groups results.

		Pre - Test		Post - Test		Within Groups		Between Groups
		Mean	SD	Mean	SD	p value	Effect size	p value	Effect size
Hip İnternal Rotator Muscles
	Virtual Golf	0.9	0.8	1.1	0.9	0.157	0.471	0.051	0.447
	Traditional Golf	0.8	0.9	0.6	0.7	0.157	0.447
Hip Flexor Muscles
	Virtual Golf	0.2	0.4	0.2	0.4	1.000	0	1.000	0
	Traditional Golf	0.3	0.5	0.3	0.5	1.000	0
Hip Adductor Muscles
	Virtual Golf	0.9	0.6	0.6	0.5	0.180	0.447	0.276	0.250
	Traditional Golf	0.6	0.8	0.6	0.8	1.000	0
Quadriceps
	Virtual Golf	0.3	0.5	0.3	0.5	1.000	0	0.081	0.400
	Traditional Golf	0.8	0.8	0.5	0.5	0.083	0.547
Hamstring
	Virtual Golf	0.6	0.7	0.3	0.5	0.157	0.471	0.478	0.163
	Traditional Golf	0.3	0.5	0.2	0.4	0.317	0.316
Gastrocnemius
	Virtual Golf	3.0	1.4	3.0	1.5	1.000	0	0.054	0.442
	Traditional Golf	3.5	1.0	3.0	1.2	0.025*	0.707
Soleus
	Virtual Golf	3.0	1.5	3.0	1.5	1.000	0	0.038*	0.477
	Traditional Golf	3.3	1.3	2.9	1.3	0.046*	0.632

Notes: for p < 0.05

A large effect size of twelve weeks of golf training was estimated for the GMFM-88, lateral step-up, curl-up, sit-and-reach, 6-min walk, and eyes-open balance tests, while a small to medium effect size was observed for the Modified Thomas and eyes-closed balance test in both virtual and traditional golf groups. The traditional golf training group exhibited a larger effect for the affected side lateral step-up test than the virtual golf training group. The estimate of effect was larger in favor of the virtual golf group for the eyes-open balance tests.

Discussion

This study aimed to evaluate the effectiveness of twelve-week traditional and virtual golf training programs on motor functions of children with CP. To our knowledge, this is the first study that investigates the effects of golf training in children with CP. We found that both traditional and virtual sports training programs in children with unilateral spastic CP have positive effects on GMFM-88, curl-up, lateral step-up, sit-and-reach, and six-minute walk tests. Participation in the twelve-week virtual golf training program was associated with significantly greater improvement in balance compared with the traditional golf training program. On the other hand, the traditional golf training group had higher positive change for ankle muscle spasticity. These findings were consistent with the previous studies examining the effects of traditional sports programs and virtual reality games on motor functions in children with CP (Dimitrijević et al., 2012, Tseng et al, 2013, Christensen et al, 2017, Chen et al., 2018).

The benefits of physical training for improving GMFM-88 scores in children with CP have been confirmed by the popular functional therapy methods such as aquatic and horse-riding interventions (Dimitrijević et al., 2012, Lai et al., 2015, Tseng et al., 2013, Whalen and Case-Smith, 2012). In this study, traditional and virtual golf training has provided positive change on the GMFM-88 scores of children with CP, which is consistent with the aforementioned studies. The golf swing requires a synergetic motor control strategy using multiple joints. The sequential pattern of muscle activation from lower to upper extremities during the golf swing may have improved gross motor functions in CP. This study also shows that virtual and traditional golf training programs have similar effects on GMFM-88 scores of children with CP. Therefore, if needed, virtual golf training may be incorporated as an alternative to traditional golf training. Golf training programs may provide functional independence, which is essential for increased participation in daily life activities via decreased motor limitations (Dimitrijević et al., 2012, Schlough et al., 2005).

Previous studies have shown that virtual reality based intervention resulted in significant improvement in COP sway parameters (Brumels et al., 2008, Gatica-Rojas et al., 2017). However, Ramstrand and Lygnegård (2012) found that the virtual reality interventions did not result in an improvement on balance. We speculate that these conflicting findings can be the result of heterogeneous sample sizes, different study designs, unsupervised interventions, and low intensity of training. In this study, twelve weeks of virtual golf training were found more effective than traditional golf training on static balance, as it decreased COF area. This result is consistent with studies reporting the superiority of virtual games on balance control (Brumels et al., 2008, Gatica-Rojas et al., 2017). Researchers introduced that, the intense repetition of motor tasks, visual feedback, and self motivation are the advantages of virtual reality interventions over traditional training methods on balance (Machado et al., 2014, Gatica-Rojas et al., 2017). During virtual golf training, participants move by receiving concurrent visual feedback from the on-screen images of themselves with gesture-based interactions. Therefore, virtual golf training can be suggested as an effective, motivating, and safe complementary exercise method for improving balance in children with unilateral CP.

In this study, both virtual and traditional golf training improved abdominal muscle strength and endurance in children with unilateral CP. The golf swing is considered to enhance abdominal muscle strength and endurance, as it includes dynamic trunk flexion and extension with rotational movements (McHardy and Pollard 2005), which requires activation of core muscles (Lim et al., 2002). Traditional and virtual golf training programs have also positively affected the lower extremity strength. It is thought that the weight transfer to the affected side and then to the non-affected side during the golf swing may increase the lower extremity strength bilaterally. The use of a heavier golf club in the traditional golf training may be a factor in creating a positive difference on the affected side lower extremity strength when compared with the virtual group.

This study showed that traditional golf training has reduced ankle spasticity similar to the conventional exercise methods (Papavasiliou, 2009). The fact that traditional golf training decreased gastrocnemius and soleus spasticity may be due to the golf club and body weight transfer to the affected side while back swinging the golf club. Prior research indicates that weight bearing based exercise had a significant reduction in ankle spasticity in children with CP (Pin, 2007). Since spasticity is dependent on velocity, it may increase in high-speed movements (Van der Krogt et al., 2009). However, this study indicates that golf training programs have no negative effect on lower extremity spasticity. Therefore, both virtual and traditional golf training may be suggested for children with unilateral CP.

Improving flexibility of these children can help increase mobility (Uzun, 2013) and activity participation (Tatar, 2010). Increased sit-and-reach test scores in both virtual and traditional golf groups indicated the positive effect of golf training programs on flexibility. Thoraco-lumbar mobility improved by repeated golf swing movement could be the reason for increasing the sit-and-reach score in both golf groups. During the golf swing, the hip joint moves from flexion to extension with trunk rotations. Although insignificant, this movement may have provided positive change on Modified Thomas Test. As prior research that examines the effects of exercise programs have not used the Sit-and-Reach and Modified Thomas Tests, the results of this study were not compared with those studies.

In this study, both the virtual and traditional groups displayed a significant increase in six-minute walk distances. The 6MWT assessment provides information regarding individual change in endurance for walking activity over time (Fiss et al., 2019). Although golf training does not include walking and running, regular golf playing enabled to increase the walking capacity of children with CP. Regular physical activity in a virtual environment also improved aerobic endurance similar to traditional sport activities (Hurkmans et al., 2010). The positive effect of virtual golf training on aerobic endurance is valuable as it increases the participation of children with CP, who have a less active lifestyle than their peers (Maher et al., 2007). In addition, the factors that contribute to 6MWT maybe not only increase in cardiovascular fitness but also increase in muscle strength/endurance and dynamic balance which resulted from repetitive golf swing and maintaining posture during the training. Similarly, previous studies have shown that muscle strength and balance have an influence on 6MWT performance in cerebral palsy (Pradon et al., 2013, Brien and Sveistrup, 2011).

Limitations

The problem of transferring participants to the training center led to a small number of participants to be included in the study. The children with unilateral CP were able to play golf without the need for any assistive equipment as they could stand without support (GMFCS I & II). However, for non-ambulatory children with higher GMSFCS levels, it may not be possible to apply the golf training or require assistive equipment.

Conclusions

This study indicated that the twelve-week golf training program for children with CP demonstrated progression in the lower extremity and abdominal muscle strength, flexibility, and aerobic endurance in both groups. This study shows the importance of participation in sports to improve the motor performance of children with CP. We believe that different exercise methods, such as virtual reality and different types of sports, will help children with CP to create more accurate movement patterns by increasing their functionality. Improving the motor performance of children with CP will also increase sports participation and improve the quality of life. Virtual training programs provide similar motor developments as traditional golf training, which needs large physical space and expensive equipment. Thus, with virtual training programs, golf is made easy to perform. Recreational features of both types of golf training will contribute to sustainability greatly. As a result, virtual reality and traditional golf training programs are supporting methods that can be used to increase the effectiveness of physical therapy and rehabilitation programs in children with CP. Furthermore, the virtual golf programs can provide an opportunity to participate in sports for these children who are unable to attend rehabilitation and sports programs.

Conflict of interest

The authors declare that there is no conflict of interest.