The Effect of Tai Chi Chuan Training on Stereotypic Behavior of Children with Autism Spectrum Disorder

This quasi-experimental study investigated effects of Tai Chi Chuan training on stereotypic behavior of children with autism spectrum disorder. Twenty-three participants (mean age = 9.60 ± 1.40 years) were assigned to experimental (N = 12) and control (N = 11) groups. The experimental group received 12 weeks of Tai Chi training and all participants had pre, post, and one-month follow-up assessments. Stereotypic behavior measured using Gilliam Autism Rating Scale 2 Scores, was significantly altered by ~ 25% in the Tai Chi Chuan group. Behavioral change was maintained at follow up since there was no significant difference between that and the posttest. In conclusion, Tai Chi Chuan training is a useful and appropriate intervention to modulate behavior in individuals with autism spectrum disorder.

Keywords: Autism; Stereotypic behavior; Tai Chi Chuan; Exercise

Autism spectrum disorder (ASD) is a neurodevelopmental disorder with a prevalence of about 1.1% in children aged 3–17 years (Perou et al., [32]). ASD is seen in 1 in 42 births for men and for women 1 in 189 births (Atladóttir et al., [1]). Children diagnosed on the autism spectrum show disorders in communication and social interaction and display repetitive patterns of behavior (Eisenmajer et al., [8]). Stereotypical behaviors are most commonly studied since they have large impacts on activities of daily living and have historically been looked to for remediation with therapy (Horner et al., [13]).

Stereotypic behaviors are repetitive, unchangeable, immutable (Baumeister & Forehand, [3]; Matson et al., [27]). These include, for instance, rocking and flapping hands, persistent use of supporting toys, looking at objects inappropriately, and oral fixation on objects. They can also manifest as seemingly harmless repeated object manipulation and repetitive use of sounds and vocalizations (Joosten et al., [16]).

Therapeutic interventions to reduce stereotypical behavior are critical to enhance and support development, especially of children, on the autism spectrum. Speech therapy, occupational therapy, and other behavioral interventions can have positive effects on stereotypic behavior in children with autism spectrum disorder (de Boer et al., [7]) but typically are very intensive and take a long time (Horner et al., [13]) and are not commonly found in all communities. The associated financial burdens are such that many families cannot afford to effectively participate in ongoing therapy. Accessible therapies that exist already in the community and that show collateral improvements in behaviors that are not directly targeted during intervention may be effective (Koegel et al., [20]). Pivotal responses are a group of specific intervention goals with the potential to include a wide range of simultaneous behavioral changes. Acquisition of a pivotal response is theorized to decrease learned helplessness and increase motivation to respond to social and educational stimuli (Koegel et al., [19])

Lavovaz and colleagues (Lanovaz et al., [21]) reviewed 60 studies aimed at a reduction in stereotype and reported that a decrease in the targeted form of stereotype in most cases resulted in a desirable increase in adaptive behavior and in a few cases an undesired increase in others stereotypes. Ledbetter-Cho et al. (Ledbetter-Cho et al., [22]) showed that collateral increase in play is often reported following interventions targeting stereotypy and conversely, a collateral decrease in stereotypy is often found following intervention targeting play.

Studies show that exercise-based interventions can be beneficial for children with autism spectrum disorder (Silva et al., [43]; Tarr et al., [46]). This may be because physical activity interventions are often generalized to include aspects such as social skills, stress reduction and not simply targeted stereotypic interventions.

Physical activity can reduce stereotyped behaviors in people with autism (Bahrami et al., [2]; Kern et al., [17]; Powers et al., [33]; Reid et al., [38]; Watters & Watters, [50]). The role of exercise intensity remains uncertain. Evidence suggests higher intensity may be more effective than mild exercise in reducing stereotypical behaviors (Kern et al., [18], [17]; Levinson & Reid, [23]), yet other work suggests this could increase in stereotypic behavior (Schmitz et al., [41]). Since mild exercise might mean greater participation and adherence, there is a need to understand better its effects.

Mind–body exercises that focus on mindfulness and purposeful connections between brain and body such as meditation (Radhakrishna, [34]) are mild intensity activities. Studies on the effectiveness of mind–body interventions in people on the autism spectrum have included yoga on maladaptive behavior and imitation skill (Chan et al., [6]) and Nei Yang Gong, a Chinese mind–body exercise. Four weeks of Nei Yang Gong improved self-control in 6–17 year olds with ASD (Rodrigues et al., [39]). The mindful practice of attention in the present moment and deliberate actions may help regulate attention and the results of this study showed that mindfulness training can lead to decrease aggressive behavior in adolescents with autism spectrum disorder (Singh et al., [44]).

Mind–body training has a long history in Asia and in China especially where internal martial arts practices like Tai Chi Chuan is a key exemplar. This training is originally a martial art focused on the promotion of balance, proprioceptive functions and body awareness (Oh et al., [29]). Experimental evidence suggests such training can improve cognition, enhance balance and reduce behavioral problems of people with autism spectrum disorder (Gatts, [10]). The main parts of Tai Chi Chuan include slow movements and balance exercises in an integrated whole-body set of actions. Tai Chi Chuan might be a useful therapeutic treatment for symptoms of children with behavioral disorders such as attention deficit hyperactive disorder, which presents with characteristics similar to those found in ASD. Especially important is that martial arts like Tai Chi Chuan are readily found in most communities, are relatively inexpensive, and easily accessible. It was shown that six-weeks of Tai Chi Chuan training can improve balance and motor coordination in children with autism spectrum disorder (Sarabzadeh et al., [40]) and also previous research has been shown that 14-weeks of Japanese karate kata training can decrease stereotypic behavior (Bahrami et al., [2]). Since any corresponding effect of Tai Chi Chuan training on stereotypic behavior of children with autism spectrum disorder remains little documented, our purpose was to examine such effects after a 12-weeks intervention.

Twenty-three children (mean = 9.6 ± 1.4 years) were recruited from an institute for children with autism spectrum disorder and served as participants under a protocol approved by the Committee on Ethical Considerations in Isfahan University. All participants were diagnosed as on the autism spectrum by a clinical psychologist. These participants had previously received applied behavioral analysis (ABA) intervention treatment (a behavioral therapy based on the encouragement of true actions) (Bootzin, [4]) for at least one year. Parents of potential participants provided informed written consent for their children to participate in the Tai Chi Chuan program before starting. Inclusion criteria included: prior diagnosis of autism spectrum disorder; age range 6–12 years old; prior history of ASD for at least 1 year; absence of comorbidities such as Down's Syndrome; requisite physical and cognitive abilities to participate; absence of prior martial arts experience. Intelligence quotient (IQ) was estimated by Ravens test and all of the participants of this study had 70 and above. Their physical abilities were estimated from their parent reports on whether their children had any problems which would restrict their participation. Participants were paired based on age, gender and severity of the disorder and then randomly assigned to Tai Chi Chuan (n = 12, 2 girls and 10 boys) or control (n = 11, 9 boys and 2 girls) groups.

The experimental group participated in a program of 45-min Tai Chi Chuan training sessions delivered three days a week (even days, afternoon) for 12 weeks. The training protocol consisted of a 10 min warm up, 25 min Tai Chi Chuan forms training and finished with 10 min cool-down. Six forms (1–6; wild horse, Grasp the sparrow's tail, wave hands in clouds, play the guitar) of Yang style Tai Chi Chuan. This protocol was based on abilities of the participants. All participants practiced together with one instructor and two assistants. During the training sessions, participants were asked to mimic the movements and posture of the teacher and follow along. In the design of the sessions attempts were made to include confidence, motivation, responding to external demands, predictability, stimulate objects to similar objects which are more tangible to children and they can see every day in their daily life routine for instance we stimulate the movement of hands into movement of clouds in the sky. If they participated in the class and mimicked the actions of the coach, at the end of the class they received a prize. Coaches provided ongoing encouragement in words, by physical guidance, patterning and attention cues, section-by- section practice.

Stereotypic evaluation was accomplished using the subscale of the Gilliam Autism Rating Scale Second Edition (GARS-2) (Montgomery et al., [28]), widely used in educational planning and research (Owens et al., [30]). The GARS-2 stereotype sub-scale included 14 items describing specific and elaborate behavioral stereotypes. The scale incorporates observation, parent or teacher questions asked by interviewers and therapists they monitor the child for three days and answer the question of the questionnaire. For each question, a 4-point rating was given based on objective frequency. The items in the subscale indicate how often parents have seen these behaviors in their children: avoiding eye-contact; fixated gaze on finger or object; quickly flipping fingers; only consume specific foods; eating inedible items; excessive smelling of objects; circular spinning; shaking the arms in a wing like motion; rapid lunging; prancing; flapping hands; making loud sounds and utterances; biting. Higher scores indicated larger levels of stereotypy.

The Ravens test included abstract images which create a logical sequence and was administered separately (Raven et al., [36]). This test has a high level of validity (0.80) and can be administered in groups (Raven & Rust, [37]). This tool in the study was used to measure cognitive abilities of participants and homogeneity of participants between control and Tai Chi Chuan groups.

We administered the stereotyped Gars-2 subtype prior to (pre-intervention), upon completion of 12 weeks (post-intervention), and during a 1-month follow-up interview with parents of participants. We administered stereotypic subscale of GARS-2 via in person interview with parents, caregivers and teachers as well as by direct observations of each participant. Prior to interviews parents and teachers discussed their ratings and reached consensus on a set of joint ratings.

Quantitative data were evaluated using SPSS version 20 software, and statistical analysis was performed using ANCOVA to determine differences between control and experimental groups. Furthermore, we used paired sample T-tests to determine whether the results were maintained at follow up after the intervention. Alpha level was set at p < 0.05.

Stereotypic behavior was reduced as a result of Tai Chi Chuan training (see Fig. 1). There was a significant difference between Tai Chi Chuan and control groups at post-test whilst controlling pre-test scores [F(1,20) = 16,536, P = 0.001, EF = 0.453]. To investigate the change in stereotypy severity in the Tai Chi Chuan group, we compared the mean score of stereotype subscale GARS-2 that individuals in the Tai Chi Chuan group achieved in pre-intervention time with the mean score post-intervention. As can be seen in the violin plots in Fig. 1a for Tai Chi Chuan and Fig. 1b for Control, there was a clear shift in the distribution of scores from pre to 3 days post only for the trained Tai Chi Chuan group. This is shown in relative terms as percentage changes from pre study values in Fig. 1c. We found a significant decrease from pre- to post-intervention (M = 12.08 + 6.097) by an average of 3.25 points (see examples of individual scoring pre and post intervention in Table 1). No significant difference was seen for the control group. The control group was initially tested in the pre-intervention (M = 11.81 + 9.29) time and then in the post-intervention time (M = 12.81 + 9.27) by an average of 1.00 points.

Graph: Fig. 1 Changes in stereotypy as a result of Tai Chi Chuan training. Violin plots show individual and group mean (dotted horizontal lines) data for Tai Chi Chuan (a filled symbols; c filled bars) and Control (b open symbols; c open bars) participants at pre intervention and 3 days and 1 month post intervention time points. *p < 0.001, NS non-statistically significant

Table 1 Single participant stereotypy scores pre and post Tai Chi Chuan training

To investigate whether the results obtained in the post-intervention persisted at follow up, we compared the post- intervention mean scores of the Tai Chi Chuan group with its mean score one month later (see Fig. 1). We found no significant difference [t(11) = 0.153, p = 0.881] since average stereotypy severity scores decreased from the post-intervention time (8.83) to the follow-up time (8.58) by an average of only 0.25 points. We also found no significant difference for the control group [t(10) = − 0.896] where the mean stereotypy severity scores increased from the pre-intervention time to the follow-up time by an average of 1.1 points.

The main result here was significant beneficial effects of mild exercise Tai Chi Chuan training on modulating stereotypic behavior in children with autism spectrum disorder that persists for at least 1-month after completion of training.

Beneficial effects of mind–body exercises such as Tai Chi Chuan in the general population have been suggested to include modulation of neuroendocrine system including effects on serotonin and the stress hormone cortisol (Jin, [15]). Overall stress reduction is a probable outcome after Tai Chi Chuan training (Matousek et al., [26]). Chronic stress can affect health of hippocampal neurons (Li et al., [24]), and one of the observations in children with autism spectrum disorder is difficulty learning and remembering new things (Lytle & Todd, [25]). Evidence suggests that physical activity can lead to reduced stress and growth of hippocampal cells (Van der Borght et al., [48]). In mind–body exercises, especially martial arts, there is forced concentration on the movements (Goldberg, [11]). Furthermore, Tai Chi Chuan exercise may lead to decreased sympathetic nervous system activity and increased parasympathetic activation (Hsu et al., [14]). Typically in children with autism spectrum disorder, there is dysfunctional regulation of parasympathetic tone compared to neurotypical adolescents (Schoen et al., [42]). Activities that can reduce stress and modulate autonomic nervous system balance are thus of potential therapeutic benefit in ASD. Although not measured in the current study, previous research using marital arts like Tai Chi Chuan show effects on cortisol levels and may stabilize serotonin levels (Jin, [15]). It is also notable that martial arts training in jujutsu has shown to increase the release of oxytocin (Rassovsky et al., [35]). It is possible that additional socially beneficial effects of traditional martial arts in those on the autism spectrum may be related to the moderating social effect of this peptide hormone. This underscores the potentially therapeutic applications of these methods for disorders involving social dysfunction, such as autism, conduct problems, or schizophrenia. The influence of these and other factors in those with ASD requires further study.

There is evidence of structural abnormalities in the basal ganglia and cerebellum in people with autism spectrum disorder Based on functional imaging studies, long-term Tai Chi Chuan training can lead to increased volume of gray matter and improved cerebellar function in humans (Tao et al., [45]). Possibly our 12-weeks of Tai Chi Chuan training led to changes in brain morphology of children with autism spectrum disorder (Calderoni et al., [5]; Hallahan et al., [12]) since a suggested contributer to stereotypical behaviors is thought to be structural differences in these areas. Future work using neuroimaging would be useful in this regard.

Tai Chi Chuan training also has an aerobic exercise component (Taylor-Piliae, [47]), even at low intensity. Stereotypic behavior in children with autism spectrum disorder is thought to be related to the inactivity of different regions of the brain (Gao & Singer, [9]). Thus this may contribute to decreasing stereotypic behavior in these children (Tarr et al., [46]). Previous research showed that vigorous physical activity led to decreased stereotypic behavior in ASD and it was suggested that fatigue could be a factor (Levinson & Reid, [23]). In this study the post-intervention assessment was three days after the last Tai Chi Chuan session thus the reduction in stereotypic behavior cannot be explained by fatigue. Furthermore, early work (Schmitz et al., [41]) showed that mild intensity movement can lead to decrease in stereotypic behavior and our result supports this.

At follow-up one month after training finished, the effects of Tai Chi Chuan training persisted. This result had been suggested previously in anecdotal reports (Zehr, [51]). According to this hypothesis, martial arts training interventions may stabilize motor control in children with autism spectrum disorder by aligning deliberate actions with anticipated sensory feedback. In martial art exercises every step and movement is the sign and trigger for the next movement in an ongoing chain. With stereotypic movement the trigger is internal and repeated. It is suggested that the contrast between external and inner sensorimotor cues may help break the internal reverberation and drive positive neuroplasticity in the direction of movement stabilization. While this may explain why the children in the Tai Chi Chuan group reduced their stereotypic behavior, it requires further experimental exploration.

The essential nature of martial arts training as found in Tai Chi Chuan exercise is balanced coordination of accurate limb movements combined with complex and integrated whole body movement (Wang et al., [49]). Coordinated whole body movements in postural and locomotor activities are inherent properties of human movement (Zehr et al., [52]). An important substrate for inter limb coordination is somatosensory feedback, especially from skin fields in the hands and feet (Pearcey & Zehr, [31]). With this in mind, it has been suggested anecdotally (Watters & Watters, [50]; Zehr, [51]) that physical activity which includes motions similar to that found in stereotypic movement patterns but which are deliberately generated as part of an intentional motor task may provide similar sensory feedback that may stabilize stereotypy. Our results are consistent with this idea but further work is needed to expand and extend these concepts Additionally, according to the pivotal response treatment theory (Koegel et al., [19]), interventions with aims not directly focused on suppressing stereotypic behavior is more beneficial for improving and decreasing stereotypic behavior. In Tai Chi Chuan training is not directly focused on reducing stereotypic behavior and can be considered somewhat similar to play for children. Our results are consistent with this idea but further work is needed to expand and extend these concepts. In future research the use of additional measurement tools such as video-recording, whole body accelerometry and enhanced recording of actual performed movements could be useful.

Mild martial arts mindful action such as contained in Tai Chi Chuan training can reduce stereotypic behavior of children with autism spectrum disorder. Future studies should examine different kinds of mind–body physical activity training (e.g. different forms of martial arts such as other "internal" systems related to Tai Chi Chuan like Bagua Zhang or Hsing-I Chuan and other "harder" styles like karate or Tae Kwon Do) the specific effect of intensity of practice on stereotypic behavior of children with autism spectrum disorder along with neurophysiological and functional measurements with larger sample sizes.

We thank all children and their families who participated in this study. We would also like to express our appreciation to the staff at Parnian Autism Institute and Dr. Shila Safavi for their support in the process of conducting this study. The authors gratefully acknowledge the assistance of Hajer Mustafa in prepration of the figures. Many thanks go to Ms. Soosan Mohajerin for her patience and kindness in instructing the children.

Ms. RT contributed to, designing the study, data collection, and data analysis, literature search, creating table and online sources. She also worked on writing the manuscript. Dr. MNA acted as the corresponding author, designing the experiment and conception, critical revision of the article, Dr. AM help in the conception and designing of this study. Dr. EPZ plays a significant role in the critical revision, editing, and writing of the article, Figure, and table. Dr. SF helped in the conception and design of this study. All authors contributed to the final approval of the version to be published.

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