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International Journal of Health Systems and Translational Medicine

Volume 1 • Issue 1 • January-June 2021

Effect of Yoga Therapy on Neuromuscular


Function and Reduction of Autism Severity
in Children With Autism Spectrum Disorder:
A Pilot Study
Soccalingam Artchoudane, Center for Yogic Sciences (CYS), Aarupadai Veedu Medical College and Hospital (AVMC &
H), Vinayaka Mission’s Research Foundation (VMRF), India
https://orcid.org/0000-0002-7826-0430

Meena Ramanathan, Centre for Yoga Therapy Education and Research (CYTER), Sri Balaji Vidyapeeth, India
Ananda Balayogi Bhavanani, Centre for Yoga Therapy Education and Research (CYTER), Sri Balaji Vidyapeeth, India
Partheeban Muruganandam, Department of Psychiatry, Aarupadai Veedu Medical College and Hospital, India
Lakshmi Jatiya, Department of Physiology, Aarupadai Veedu Medical College and Hospital, India

ABSTRACT

Autism is characterized by dysfunction in motor execution and sensory perception that are linked with
neuromuscular function (fN) for children with autism spectrum disorder (ASD). This article aims to
evaluate effectiveness of yoga therapy (YT) on fN and autism severity in children with ASD. Sixty
children were screened (age 6 to 18) using childhood autism rating scale (CARS); 40 were allocated
randomly (n=20) into yoga (YG) and control (CG) groups; both followed regular school routine,
and YG received 10 YT sessions (60 min/session). Visual reaction time (VRT), handgrip strength
(HGS), and CARS were measured. YG showed significant changes in VRT and CARS after YT
and intergroup comparisons revealed significant differences between groups at the end of the study
(VRT,p=0.008; CARS,p=0.011). YT resulted in small but statistically significant changes in CARS
and significant improvement in VRT. This implies that YT can be used as an adjuvant modality for
children with ASD, reducing co-morbidities with regard to the neuromuscular function.

Keywords
Cognition, Integrated Yoga Therapy, Mindfulness-Based Practice, Neurodevelopmental Disorder

INTRODUCTION

Autism spectrum disorder (ASD) is a complex neurodevelopment disorder with estimated prevalence
rate of 61.9/10,000 globally, 1% in the United Kingdom, 1.5% in the United States and it has been
estimated that more than 2 million people may be affected with ASD in India (Chauhan et al., 2019).
The core characteristics of ASD are impairments in cognition, communication, social-interaction,

DOI: 10.4018/IJHSTM.2021010104

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restricted and repetitive or stereotyped behaviours. The multisystem fragility is prone to proprioceptive
and motor coordination dysfunction and thus it causes trauma and chronic pain. The inter relation
between musculoskeletal disabilities and hypermobility-related disorders is disregarded in the ongoing
system of specialization of care by various medical fields although both conditions usually occur
simultaneously more often than for this to be a coincidence (Baeza-Velasco et al., 2018).
It is mentioned in Thirumandiram, a classical tamil text on yoga, “Maadha udharam malamigil
mandanaam, maadha udharam jalamigil moongaiyaam, maadha udharam irandokkil kannillai,
maadha udharatthil vanda kuzhavikke” (Thirumandiram, 465), which means, during intercourse if
the female has heavy bowels then this leads to impaired cognition in the infant; if her bladder is full
then this leads to speech disorders in the infant; if her bowels and bladder are both heavy then this
leads to blindness in the infant (Natarajan, 2002). This may be due to chromosomal alterations and
neurodevelopmental plasticity in the offspring (Gluckman et al., 2009). Heavy bowels or bladder
which can be attributed to dysfunction in elimination process is mainly due to the psychopathology of
stress. Several subclinical physiological changes with respect to maternal stress have been described,
including alterations in immune, brain, cardiovascular, autonomic, endocrine, and metabolic functions,
such as changes in fetal heart rate, insulin resistance, increased concentrations of immunoglobulin
E in cord blood and changes in hypothalamic–pituitary–adrenal (HPA) axis function (Monk et al.,
2011; Entringer et al., 2008; Lin et al., 2004). Variations in HPA axis activity have also been linked
with other diseases, such as mental disorders, respiratory diseases, diseases of the skin, and infectious
diseases (Buske-Kirschbaum et al., 2010; Priftis et al., 2009).
The primary purpose of this study was to measure the effectiveness and feasibility of yoga
therapy, both quantitatively through handgrip strength (HGS) and visual reaction time (VRT), and
qualitatively through high functioning Childhood Autism Rating Scale, second edition (CARS2-HF)
in children with ASD. Foley (2018) found that yoga along with complementary alternative medicine
(CAM) increases attention, awareness, self-control and decreases anxiety and self-stimulatory actions.
It has been shown that yogic techniques such as jattis, kriyas, asanas and pranayama help improve
physiological functions, loco-motor skills, psycho-motor coordination, attention and sleep in children
with ASD (Ramanathan & Bhavanani, 2018; Ramanathan et al., 2019).
Several studies have reported that there was higher incidence of hypotonia and ataxia, poorer motor
skills in children with ASD (Travers et al., 2017). Kern et al. (2013) found that handgrip strength is
significantly poorer in such children. The empirical facts and evidences to support the effectiveness
of yoga therapy for individuals with ASD are inconclusive. The authors have also reviewed the
benefits of yoga which are as follows i) improves muscle strength by decreased sympathetic activity
and autonomic arousal; ii) improves cardiac vagal tone by reduced blood pressure and external
stimuli; and iii) improves sensory process, behavior, social communications in children with ASD
(Artchoudane et al, 2019). Semple (2019) reported that yoga practices have some positive effects
on social communication, emotional stability, and overall behavior in individuals with ASD. It is
suggested that Yoga may be superior to physical exercises such as aerobics, walking, running, dancing
and cycling as compared in reviewed studies, on psychological, social, environmental, occupational
functioning measures of quality of life (Streeter et al., 2010). Several studies have found asanas to be
highly beneficial when practiced as physical activity as it promotes energy conservation and enhances
quality of life in individuals with ASD who practice on a regular basis (Reinders et al., 2019). Yoga
practices help increase positive feelings, alertness and decrease negative feelings of anxiety, depression
and aggressiveness; and help regulation of blood glucose levels and improve cardiovascular system
(Danhauer et al., 2017; DeBruin et al., 2017; Amaranath, Nagendra, & Deshpande, 2016; Klainin-
Yobas et al., 2015; Yadav et al., 2015). Pranayama with rapid paced breathing, bhastrika, mukha
bhastrika, or kapalabhati increased activity of beta-adrenoceptors which help increase cardiac vagal
tone; and reduced anticipatory responses which improve neurocognitive, autonomic and pulmonary
functions as well as biochemical and metabolic activities in the body (Saoji, Raghavendra, &
Manjunath, 2019; Bhavanani, Ramanathan, & Harichandrakumar, 2012).

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The purpose of this pilot study is to investigate if and how yoga can influence specific components
of issues related to neuromuscular coordination and neurological response in children with ASD; to
check the feasibility of a long term study in this population, as well as to verify if such training could
possibly reduce the severity in autism rate. It is hypothesized that regular, repeated practice of yoga as
therapy for children with ASD will enhance measures of neuromuscular coordination and neurological
responses. Thus, through expanded effect of yoga therapy the capacity for musculoskeletal ability
and sensory integration may increase.

MATERIALS AND METHODS

Subjects
Study participants were 40 children (32 boys, 8 girls) aged 6 to 18 years (mean=13.9, SD=1.75). The
convenient sample of children with ASD was from Satya School, one of the schools providing care for
children with special needs in Pondicherry, India. All the children were screened for clinical diagnosis
of ASD and selected by psychiatrist physician using CARS2-HF for autistic disorders (Novakovic
et al., 2019). Additionally they received the diagnosis of autism according to the CARS2-HF which
was also an inclusion criterion. Children receiving standard school routine were eligible if they would
be present with regularity for the duration of the trial. They were excluded if they had significant
behaviour problems, marked mental retardation, visual or auditory impairments, uncontrolled seizures
and using postural assistive devices. Children who had CARS greater than 15 were enrolled.
Approval was obtained from Institutional Research Committee (AV/IRC/2019/03), Institutional
Human Ethical Committee (AVMC/IEC2019/031) and registered in the Clinical Trials Registry - India
(ICMR-NIMS) REF/2019/07/027443. Approval and written consent was also obtained from authorities
of the Special School as well as parents or guardians of the children who participated in the study.

Study Tools

• Anthropometric data: Individual height was measured to the nearest centimetre by a wall mounted
stadiometer and weight measured with a weighing scale (Krup’s scale). BMI was calculated by
Quetelet’s index that is weight (in kg)/ height (in sq. m).
• Musculoskeletal function data: Musculoskeletal function test is to measure the maximum isometric
strength of the hand and forearm muscles. Handgrip dynamometer - JKA-315 by Microteknik
was used to measure handgrip strength in kilogram per second and not affected by temperature
change, pressure change, condensation etc.
• Neurological function data: Neurological function test was used for measuring visual response that
is time taken for visual stimuli per second by using Reaction time (RT) apparatus manufactured by
Anand Agencies, Pune. The instrument has inbuilt 4 digit chronoscope with a display accuracy of
1 millisecond and featured with a ready signal, four stimuli and two response keys. It has switches
for selecting left or right response key for respective stimuli provided. In the present study VRT
was tested for red light stimulus. The children were instructed to release the response key as
soon as they perceive the stimulus. Visual signals were produced right in front of the subjects
to avoid the effect of lateralized stimulus and they used their dominant hand while responding
to the signal. The RT apparatus has an electronic four digit display and works on 230 volts A.C.
• Autism rate: High Functioning Childhood Autism Rating Scale, second edition (CARS2-HF)
was used for quantitative results, an autism-specific instrument designed to rate the behaviour,
intensity, peculiarity and duration. There are fifteen questions with seven possible responses,
scored from 1-4, increasing by .5 (i.e., 1, 1.5, 2, 2.5, etc.). It determines autism severity rating
values for all items that are summed to produce a total raw score where less than 15 denotes no
symptoms, 15 to 27.5 denotes minimal to no symptoms, 27.6 – 33.5 denotes mild to moderate
symptoms, and above 33.5 denotes severe symptoms.

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Table 1. Yoga therapy schedule *

Sno. Techniques Repetition (round) Duration (min)


1 Prayer: AUM chanting 3 5
2 Yogic Sukshma Vyayama (loosening practices):
     a) Katishakti vikasak (Trunk twisting) 3 3
     b) Ardha Katichakra kriya (lateral stretching) 3 3
     c) Tada kriya 4 4
3 Tadasana 2 3
4 Vrikshasana 2 3
5 Padahastasana 2 3
6 Pawanamuktasana 2 3
7 Paschimottanasana 2 3
8 Jatara Parivrittasana 2 3
9 Bhujangasana 2 3
10 Sarvangasana 2 3
11 Pranava Pranayama 3 6
12 Bhramari Pranayama 3 5
13 Shavasana 1 5
14 Prayer: AUM chanting 3 5
Total 60
* Modified according to individual ability.

Block randomized controlled trial was conducted in the period August - November 2019. CARS,
HGS and VRT parameters were recorded before the study. The children were randomly assigned to
either yoga group (n=20) or control group (n=20). Each child was guided by the yoga therapist to
practice yoga protocol. Yoga group underwent yoga therapy for 60 minutes a day; 5 days a week for 2
weeks along with regular school activities and control group attended regular school routine without
yoga therapy. After 10 sessions, post recording of CARS, HGS and VRT were done. All 40 children
were present during pre-test and post-test recording of data of the study. Parents of the children and
the investigator were unaware and had no information on participation of the children with respect
to their group; this could decrease the bias of parents in answering.

Yoga Therapy Intervention


Yoga therapy protocol designed by authors is presented in Table 1. Sessions were delivered by a
yoga therapist between 11.30 am and 12.30 pm just before lunch hour. Yoga module included guided
practice of asana, pranayama and relaxation during the sessions along with support of their teachers.
The practices performed by children with ASD were modified based on their individual ability.

STATISTICAL ANALYSIS

GraphPad InStat 3.06 analytic software for windows 7 was used to determine normality. As data did
not pass normality testing, Wilcoxon signed-rank test for dependent or matched groups and Mann-

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Table 2. Comparison of HGS, VRT and CARS2-HF between yoga and control groups

Yoga (n=20) Control (n=20) P value


Parameters
Pre Post Pre Post Pre Post
6.5 8.5 1.50 1.50
HGS (kg) 0.012 0.001
(1,19) (1,21) (1,8) (1,5)
712.29 950
864.43 910
VRT (ms) (325.33, 1510.33) (484.14, 0.579 0.008
(484.14, 1413.86) (514, 1328)
* 1387.57)
56 54.50 61.50
CARS 64.50 (40,69) 0.302 0.011
(48,68) (42,66) * (42,69)

Whitney U test for independent groups were adopted for comparison of the changes in both groups
that are given in Table 2.
Values are given as median (min, max). * p<0.05 by Wilcoxon Signed Ranks test for intra-group
comparisons and actual p values are given for intergroup comparisons using Mann-Whitney U test.

RESULTS

Results are given in Table 2. Yoga group showed significant changes in VRT and CARS after Yoga
therapy and inter group comparisons revealed significant differences between groups at the end of
the study (VRT, p< 0.008 and CARS, p<0.011). Matched median score of delta HGS was 2 kg/sec
in yoga group but there was no change in control group. As HGS values were not comparable at
baseline, positive changes that occurred in YG were not statistically significant.

DISCUSSION

Yoga therapy is a comprehensive therapy modality for children with ASD. It is ideal for improving
musculoskeletal, neurological, cardiovascular, endocrine and immune function, especially for children
with ASD, because asana practices integrate mind, body and breath (Kaduskar & Suryanarayana,
2015; Kelly et al., 2018). This integration is the central aspect of postures which in turn affect motor
and sensory processes and this further connects to anatomical and neurophysiological aspects of
stretching. Proprioceptive neuromuscular facilitation (PNF) stretching is the most effective technique
facilitating a greater experience of the asana itself. Yogasana helps to place the target muscle on stretch
followed by static contraction of the target muscle which influences the brain functions for motor and
sensory process integration through selected anatomical movements of the body with proper breath
coordination (Srinivasan, 2016; Bhavanani & Ramanathan, 2017).
The selected practices used in this study aim to focus on stimulating and stretching the muscles
in coordination with the breath which harmonises the sympathoadrenal activity and hypothalamic-
pituitary-adrenal axis (Innes & Vincent, 2007; Innes, Bourguignon & Taylor, 2005; Cusumano &
Robinson, 1993). It has been seen earlier that such a set of practices with rhythmic breathing, regularity
and repetition may enhance vagal tone, parasympathetic activity, heart rate variability and decrease
systolic blood pressure (Telles, Sharma & Balkrishna, 2014; Payne & Crane-Godreau, 2013; Brown
& Gerbar, 2005).
Every yoga therapy session started and ended with a prayer. The prayer consists of ‘AUM’ chanting
which was a slow, regular and rhythmic practice. Producing and listening to the sound helped reduce
aggressiveness in children with ASD (Ramanathan et al., 2019; Litchke, Liu, & Castro, 2018). Yogic
sukshma vyayama are warming up exercises or loosening exercises to remove stiffness of physical

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body as well as mind, and besides repetitive movement of the joints it also includes movements
similar to those of animals like cat, dog, tiger etc. with respective sounds which the children with
ASD were guided to practice.
Children with ASD in the study had higher median score of CARS in yoga group than control
group, this could be attributed to mood enhancement even in the short term intervention of 10 sessions
of yoga therapy (Litchke, Liu, & Castro, 2018). The delta median score of HGS showed improvement
in yoga group and this endorsed increased attention span (Narasingharao, Pradhan, & Navaneetham,
2017; Sequeira & Ahmed, 2012, Soccalingam, Ramanathan & Bhavanani, 2020).
VRT was significantly shortened following yoga practice and this improvement is similar to
the result obtained by Bhavanani et al. (2017) who found that asana and pranayama reduces RT by
enhancing central processing ability with effect of better awareness, alertness, sensitivity and sense
of perception in normal individuals, in special children (Artchoudane et al., 2019) and in children
with ASD (Ramanathan & Bhavanani, 2018). We have found such similar changes in this study too,
as shown in the earlier studies with short term yoga therapy and found that it is very effective for
children with autism in enhancing VRT (Baisch et al., 2017).
Authors have suggested that this improvement can influence the mechanism of sensorimotor,
frontal-striatal functions, or developmental alterations of the brainstem (Dadalko & Travers, 2018;
Bricout et al., 2019) which showed positive changes involving cognitive, motor and behavioral
functions within the brain of children with autism (Soccalingam, Ramanathan & Bhavanani, 2020).
Yogic counselling including suggestions for dietary modifications may have brought major
changes of gut microbiota function that may correlate with behavioral positive changes in children
with ASD (Liu et al., 2019; Cheng & Ning, 2019; Argou-Cardozo & Zeidán-Chuliá, 2018). The
involved model of yoga therapy includes i) dietary modification which consists of exclusion of foods
that contain excessive protein, intake of drinking water upto 3 litres at regular intervals, inclusion of
foods that contain more minerals and culinary herbs which may improve gut microbiota composition
and have beneficial repressive effects that can be assigned to increasing butyrate and propionate
biosynthesis (Liu et al., 2019; Peterson et al., 2019; van Sadelhoff et al., 2019); ii) jattis and asana
which promote flexibility and neuroimmune interactions that helps controlling immune responses
which may increase transforming growth factor beta (Ashwood et al., 2008); iii) pranayama and
relaxation which improve vital capacity and reduces stress that can be attributed to increase in anti-
inflammatory cytokines interleukin (IL) - 1 receptor antagonist, IL-10 (Saghazadeh et al., 2019a) and
decrease in pro-inflammatory cytokines interferon gamma, tumor necrosis factor alpha or TNF-α,
IL-1β and IL-6 (Saghazadeh et al., 2019b) in children with ASD. Therefore, alternate hypothesis
proved that regular and repeated yoga therapy sessions addressed specific issues on musculoskeletal
function, neurological response and brought mild positive changes in children with ASD.

CONCLUSION

This pilot study provides evidence of the feasibility of such studies in the longer term and showed
significant improvement in VRT with small yet significant changes in CARS2-HF in the children
with ASD. This may be attributed to better balance and integration of musculoskeletal function with
enhanced neurological response in children with ASD after yoga therapy. Overall improvement of
VRT can be attributed to harmonization of mind-body-emotion through yoga therapy that also helps
develop social skills and promotes self-confidence. Yoga therapy can be used effectively and safely
in this population and may be adopted as a long term adjuvant therapy to reduce severity as well as
co-morbidities related to autism.

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S. Artchoudane MSc., MPhil., PhD (ongoing) is Yoga Therapist, Center for Yogic Sciences (CYS), Aarupadai Veedu
Medical College and Hospital (AVMC & H), Vinayaka Mission’s Research Foundation (VMRF), Puducherry, India.
He has published several research papers and conference papers on yoga therapy for pulmonary, neuromuscular,
neurodevelopmental and cardiovascular disorders. He has also authored several book chapters on yoga therapy for
neurodevelopmental and inflammatory bowel disorders. He is a recipient of the Achiever’s Awards for ‘Best Yoga
Teacher’ and ‘Yuva Bharathi’. He has obtained 8 copyrights on value added courses and yoga protocols. He is a
professional member of Indian Yoga Association and member of jury, Pondicherry Yogasana Association, India.

Ramanathan Meena (PhD) is Associate Professor and Deputy Director of CYTER, the Centre for Yoga Therapy
Education and Research at Sri Balaji Vidyapeeth. She has completed numerous undergraduate and postgraduate
degrees and diplomas in Yoga, Science and English has completed her PhD in Yoga through Tamil Nadu Physical
Education and Sports University (TNPESU). She is a recognized IAYT Certified Yoga Therapist by the International
Association of Yoga Therapists, USA. She has been recognized as PhD Guide (Yoga Therapy and Interdisciplinary
Research) by Sri Balaji Vidyapeeth, Pondicherry in March 2016, appointed as Lead Examiner for Yoga Certification
Board (YCB) through Indian Yoga Association, recognized by AYUSH, Central Ministry of Health, and New Delhi
in Sep 2016. She has been nominated as “Subject Expert” in the Selection Committee of the Govt of Puducherry,
Directorate of Indian Systems of Medicine and Homeopathy; under National Health Mission. She recently received
the Achiever’s Award for “Best Yoga Therapist 2016”. She is currently a Professional and Executive Committee
member of Indian Yoga Association representing Pondicherry. She has authored and co-authored a dozen books
and more than three dozen papers on Yoga in English and Tamil in various journals. She is currently carrying on
many Research/Pilot Studies at CYTER of SBV at MGMCRI as a guide and co-guide for PhD and MPhil in Yoga
Therapy, and has published 40 scientific papers, 11 compilations and a dozen abstracts in leading Scientific Journals.

Ananda Balayogi Bhavanani (PhD) MBBS, ADY, DPC, DSM, PGDFH, PGDY, FIAY, MD (Alt.Med), C-IAYT, DSc
(Yoga) Yogacharya Dr. Ananda Balayogi Bhavanani is Director of the Centre for Yoga Therapy Education and
Research (CYTER), and Professor of Yoga Therapy at the Sri Balaji Vidyapeeth, Pondicherry (www.sbvu.ac.in).
A recipient of the prestigious DSc (Yoga) from SVYASA Yoga University in January 2019, he is a Gold Medallist
in Medical Studies (MBBS) with postgraduate diplomas in both Family Health (PGDFH) as well as Yoga (PGDY)
and the Advanced Diploma in Yoga under his illustrious parents in 1991-93. A Fellow of the Indian Academy of
Yoga, he has authored 19 DVDs and 23 books on Yoga as well as published nearly 300 papers, compilations and
abstracts on Yoga and Yoga research in National and International Journals. His literary works have more than
2400 Citations, with an h-Index of 23 and an i10-Index of 40.

M. Partheeban MBBS, MD is currently working as Assistant Professor, Department of Psychiatry, Aarupadai Veedu
Medical College and Hospital (AVMC & H), Vinayaka Mission’s Research Foundation (VMRF), Puducherry, India.
He has published several research papers in regards to Perinatal psychiatry, Addiction disorder, Geriatric psychiatry,
COVID 19 mental impact and Child psychiatry. He received awards for ‘SERWICE’ (Service for Enhanced Recovery
With Intensive and Continued Engagement) and ‘Best Psychotherapy’.

Lakshmi Jatiya MBBS, MD is Professor and Head, Department of Physiology, Aarupadai Veedu Medical College
and Hospital (AVMC & H), Vinayaka Mission’s Research Foundation (VMRF), Puducherry, India.

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