|Year : 2019 | Volume
| Issue : 1 | Page : 55-61
|Effect of yoga as an add-on therapy in the modulation of heart rate variability in children with duchenne muscular dystrophy
Dhargave Pradnya1, Atchayaram Nalini2, Raghuram Nagarathna3, Trichur R Raju4, Ragupathy Sendhilkumar1, Adoor Meghana4, Talakad N Sathyaprabha4
1 Physiotherapy Center, National Institute of Mental Health and Neurosciences, Bengaluru, Karnataka, India
2 Department of Neurology, National Institute of Mental Health and Neurosciences, Bengaluru, Karnataka, India
3 Vivekananda Yoga Research Foundation, Bengaluru, Karnataka, India
4 Department of Neurophysiology, National Institute of Mental Health and Neurosciences, Bengaluru, Karnataka, India
Click here for correspondence address and email
|Date of Web Publication||11-Dec-2018|
| Abstract|| |
Background: Duchene muscular dystrophy (DMD) is a progressive muscular disorder. Cardiac disorder is the second-most common cause of death in children with DMD, with 10%–20% of them dying of cardiac failure. Heart rate variability (HRV) is shown to be a predictor of cardio-autonomic function. Physiotherapy (PT) is advised for these children as a regular treatment for maintaining their functional status. The effect of yogic practices on the cardio-autonomic functions has been demonstrated in various neurological conditions and may prove beneficial in DMD. Materials and Methods: In this study, 124 patients with DMD were randomized to PT alone or PT with yoga intervention. Home-based PT and yoga were advised. Adherence was serially assessed at a follow-up interval of 3 months. Error-free, electrocardiogram was recorded in all patients at rest in the supine position. HRV parameters were computed in time and frequency domains. HRV was recorded at baseline and at an interval of 3 months up to 1 year. Repeated-measures ANOVA was used to analyze longitudinal follow-up and least significant difference for post hoc analysis and P < 0.05 was considered statistically significant. Results: In our study, with PT protocol, standard deviation of NN, root of square mean of successive NN, total power, low frequency, high-frequency normalized units (HFnu), and sympathovagal balance improved at varying time points and the improvement lasted up for 6–9 months, whereas PT and yoga protocol showed an improvement in HFnu during the last 3 months of the study period and all the other parameters were stable up to 1 year. Thus, it is evident that both the groups improved cardiac functions in DMD. However, no significant difference was noted in the changes observed between the groups. Conclusion: The intense PT and PT with yoga, particularly home-based program, is indeed beneficial as a therapeutic strategy in DMD children to maintain and/or to sustain HRV in DMD.
Keywords: Duchene muscular dystrophy, heart rate variability, physiotherapy, yoga
|How to cite this article:|
Pradnya D, Nalini A, Nagarathna R, Raju TR, Sendhilkumar R, Meghana A, Sathyaprabha TN. Effect of yoga as an add-on therapy in the modulation of heart rate variability in children with duchenne muscular dystrophy. Int J Yoga 2019;12:55-61
|How to cite this URL:|
Pradnya D, Nalini A, Nagarathna R, Raju TR, Sendhilkumar R, Meghana A, Sathyaprabha TN. Effect of yoga as an add-on therapy in the modulation of heart rate variability in children with duchenne muscular dystrophy. Int J Yoga [serial online] 2019 [cited 2020 Aug 12];12:55-61. Available from: http://www.ijoy.org.in/text.asp?2019/12/1/55/247138
| Introduction|| |
Duchenne muscular dystrophy (DMD) is a steadily progressive primary muscle disease and is the most common form of neuromuscular disorder with an X-linked recessive pattern of inheritance that ultimately leads to loss of ambulation and death at a young age., The incidence of DMD is approximately 15.9–19.5/100,000 live births., In India, DMD has been found to account for 30% of all reported forms of muscular dystrophies. Respiratory failure and cardiac involvement are the most common causes of death in children with DMD, but with advancement in respiratory support techniques, cardiac disorders remain an important problem in the late stages of the disease. Research in this field reveals that there is an involvement of myocardium before the onset of clinically apparent cardiomyopathy in DMD. However, it has been observed that, in a routine management of DMD children, assessment of cardiac function is not considered until the clinical manifestations are detected. Nonrecognition of cardiac impairment and treatment at the early stages can lead to poor outcomes. Hence, recognition and management of the cardiac autonomic dysfunction is an important strategy for prolonged life expectancy and better quality of life in children with DMD.
Heart rate variability (HRV) assessment is an economical, noninvasive, and sensitive procedure for investigating autonomic neurocardiac regulation. HRV also provides a novel approach to the clinical diagnosis and prognostic measures. Several authors have used HRV to assess cardiac neural regulation.,, Short-term HRV analysis is a good tool to investigate DMD children for evidence of cardiac autonomic dysfunction. Our previous study demonstrated the need for routine assessment of cardiac functions using HRV measures, and short-term HRV analysis showed significant difference in the cardio-autonomic parameters among the DMD children than the healthy volunteers.
Apart from medical management, physiotherapy (PT) in the form of physical exercise is considered as one of the vital rehabilitation strategies for the maintenance of physical function. The role of exercise has been studied in the modulation of cardiac functions and found that training induces a resting bradycardia accompanied by increased cardiac vagal modulation in healthy individuals.
Yoga being the adjuvant therapy is considered as a simple practice that can be followed even at home with prior training. Practicing yoga has shown improvement in cardio-autonomic functions in normal individuals of different age groups.,, Improvement in cardio-autonomic functions in healthy volunteers using different yoga modules and physical exercise has been documented. However, the effect of yoga therapy to modulate HRV in DMD children has not been studied.
| Materials and Methods|| |
This study was conducted at the National Institute of Mental Health and Neurosciences (NIMHANS). Approval for this study was obtained from the Institutional Ethics Committee. Two hundred children were screened, and 124 children with genetically confirmed DMD, in the age group of 5–10 years, who were self-ambulant or required minimal assistance for walking, were recruited after obtaining written assent and consent. Our cohort were drug naive at the time of evaluation and were recruited for the study after genetic testing which was available within 3–4 weeks after clinical examination. Children who had muscular dystrophy other than DMD, nonambulant children, and children/parents not willing to participate in the study were excluded from the study.
Age matched randomized controlled repeated measure design.
The patients were paired for age and randomly allocated to Group 1 (PT only) and Group 2 (yoga and PT [Y and PT]) using a computer-generated random table.
HRV was used as the assessment tool in this study. Artifact-free, electrocardiograms were obtained for all patients in the supine position. Recordings were analyzed for time and frequency domain parameters according to the Taskforce report on HRV. HRV parameters were computed in time and frequency domains. Time domain measures include the standard deviation of NN (SDNN) interval and root of square mean of successive NN (RMSSD) interval. Frequency domain consisted of total power (TP), low frequency (LF), and high frequency (HF) power values. The ratio of LF/HF power values was determined using the customized software. HRV assessments were done at the first presentation and sequentially at intervals of 3, 6, 9, and 12 months. All participants were given a compliance notebook to maintain exercise performance to make sure that children were practicing yoga and PT at home. Log books were reviewed on every visit.
All children received the standard approved therapy of oral prednisolone at 0.75 mg/kg/day from the day of diagnosis and this was continued during the entire study period.
PT exercise was taught to children and parents in the Physiotherapy Department of NIMHANS. They were made to practice it under the supervision of physiotherapists initially for a period of 1 week. Once they learned the exercises, they were advised to carry it out at their homes. PT exercises were performed twice daily by the participants, morning and evening for 45 min per session, and were continued during the entire study period. Details of PT exercises are summarized in [Table 1].
Similarly, yoga practice was taught to the children and their parents by a trained, accredited yoga therapist. They were made to perform the yoga under the supervision of the yoga therapist for 1 week. Once they learned, they were advised to practice yoga in their homes. Children in this group performed yoga in the morning and PT exercises in the evening, each session lasting for 45 min, and was continued during the entire study period. Detail of yoga practices is summarized in [Table 2].
All the data were documented in a standardized pro forma and later decoded.
Basic demographic details were analyzed using descriptive statistics. Groups were compared using independent sample t-test for continuous variables. HRV data were square root transformed to produce normal distributions. Values are expressed in (mean [standard deviation]). Level of significance was kept at <0.05. RM ANOVA was used to analyze longitudinal follow-up and least significant difference for post hoc analysis.
| Results|| |
The age of the children participated in this study ranged from 5 to 10 years. The mean age at presentation was 7.9 ± 1.5 years. Mean height was 118.2 ± 8.4 cm (95–147 cm). Mean weight was 20.6 ± 4.3 kg (11–32 kg). Mean age at onset of DMD was 2.8 ± 0.6 years (1.5–4.0 years). Mean duration of illness was 5.1 ± 1.5 years (1–8 years). At the end of the study, 45 children completed the scheduled assessments in PT group and 43 children completed in Y and PT group. Details are explained in CONSORT diagram [Figure 1].
At baseline, DMD children showed significantly lower mean NN (PT: 606.1 ± 77.1 and Y and PT: 605.7 ± 78.5), higher average heart rate (PT: 100.4 ± 12.0 and Y and PT: 100.8 ± 13.0), and significantly reduced HF and HF normalized units (HFnu). The sympathovagal balance (SVB) was tilted toward sympathetic limb in DMD children. The time and frequency domain findings of HRV were similar in both the two study groups.
After the PT protocol, SDNN, RMSSD, TP, LF, HFnu, and SVB improved at varying time points and the improvement lasted up for 6–9 months. Whereas the combined protocol of PT and yoga showed an improvement in HFnu during the last 3 months of the study period and all the other parameters were stable up to 1 year. When compared age wise with baseline values up to 1 year, in PT group, there was no significant change in any of the HRV parameters, while, Y and PT group showed a significant improvement in HFnu in 5–6 years' group and mean NN and average HR in 7–8 years. However, no significant difference was observed between PT and Y and PT groups in other parameters. We observed that PT group demonstrated improvement in HRV parameters, but these effects were not long lasting, whereas Y and PT combination is more helpful in improving cardiac function between 5–8 years of age. Detailed data are provided in [Table 3] and [Table 4].
|Table 3: Comparison of serial evaluation of heart rate variability values in the two study groups|
Click here to view
|Table 4: Age-wise difference between baseline and 1 year for heart rate variability values in the two study groups|
Click here to view
| Discussion|| |
This study was conducted to know the added effect of yoga in the modulation of HRV among the children with DMD. The HRV measures were used to assess the sympathetic and parasympathetic nervous activities. In HRV measures, the HF component of the HRV indicates the vagal activity. In a given point of time, any rise in the HF power, especially HFnu, indicates a vagal dominance. Similarly, increased LF power indicates increased sympathetic activity. The LF-HF ratio indicates overall SVB. High LF-HF ratio denotes increased sympathetic activity and a low LF-HF ratio indicates increased parasympathetic activity. In this study, the baseline HRV findings were showing predominant sympathetic overactivity (increased SVB and reduced HF; HFnu) along with decreased mean NN. Subsequently, the PT intervention showed noteworthy changes in HRV parameters. The parasympathetic domination was very obvious during the intervention and lasted up to 6–9 months. However, the added benefit of yoga showed further improvement in parasympathetic regulation (HFnu). The age-wise improvement toward vagal balance was significant in our study. There was an additional long-lasting improvement in autonomic modulation in 5–8 years of age of DMD children with Y and PT group. All these findings confirm that DMD children have autonomic dysfunction and these can be modulated by the interventions and stringent follow-ups. We also proved that yoga as an adjuvant therapy has an additional benefit in enhancing the neuro-cardiac autonomic controls.
Studies showed that skeletal muscle training can be beneficial in patients with DMD.,, Despite the lack of studies addressing the use of yoga exercises as a complementary therapy for DMD patients, there have been several other clinical studies of yoga on healthy volunteers. A study on healthy adults aimed to find out the effect of yoga practice on HRV and showed increase in certain HRV parameters such as mean RR interval, SDNN, HF power, and HFnu. There was also reduction in the resting heart rate, LF power, and LF/HF ratio. Several other studies on the effect of yoga on HRV exhibited an increase in the parasympathetic tone which is reflected through the HRV measures., To our knowledge, the present study is the first to address and confirm the safety and efficacy of yogic exercises along with PT in children with DMD. The yogic exercises used in the present study are distinctive and were aimed at improving the muscular strength. Each school of yoga has various physical postures (asanas), breathing practices (pranayama), and meditation as their components. In our study, we used Sakthivikasaka (a practice aimed to improve the overall muscular function), selected asanas, pranayama, and meditation (guided meditation). Although the effect of Sakthivikas has not been studied, it can be considered as a practice equivalent to performing moderate-intensity exercise. Since yoga comprises both physical activity in the form of sakhivikasakas and asanas and pranayama, it has advantage in the modulation of HRV through mechanisms similar to practicing physical exercises in addition to practicing pranayama and meditation.
The possible beneficiary effect of interventions on DMD may be due to several mechanisms. It includes a reduction in the catecholamine, angiotensin II, and an increased bioavailability of nitric oxide. Complex neurophysiological mechanism, mediated through limbic, hypothalamic medullary axis and the medullary cardiovascular center, is thought to be the reason for improvements in the HRV after the practice of slow pranayamas. On the other hand, HF yoga breathing practices such as Kapalabhathi are found to enhance sympathetic activity by reducing the vagal tone. Overall relaxation and calming the mind through physical and breathing practices is the primary goal of yogic practices. Finally, we could see that yoga does have a positive effect on skeleton muscle as well as neuro-cardiac beneficiary with probable above-discussed mechanisms.
Strengths and limitations of our study
To our knowledge, this is the first study involving DMD children, with follow-up for 1 year, with large samples, to study the effect of yoga. It was a longitudinal, prospective, age-matched, two-group randomized study, with controlled RM design. The DMD being a progressive disease, performing exercise and yoga might have reduced the deleterious effects on such patients. The primary objective of the study was to show that yoga and exercises can be performed by patients with DMD. Although there was 30.6% and 27.4% dropout in yoga and exercise groups, this study showed that yoga exercises are feasible, harmless, and can actually improve HRV in DMD children.
This study was not blinded for assessments and interventions.
| Conclusion|| |
Since modulation of HRV is an indicator of stable cardiac function and assessment of cardiac function using HRV measure and therapeutic measures, we advised that combined PT and yoga can be initiated as one of the rehabilitation strategies in children with DMD. This can also be a home-based PT, and yoga programs appear to be beneficial and cost-effective in the management of patients with DMD if started early.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Siciliano G, Tessa A, Renna M, Manca ML, Mancuso M, Murri L, et al.
Epidemiology of dystrophinopathies in North-West Tuscany: A molecular genetics-based revisitation. Clin Genet 1999;56:51-8.
Parsons EP, Bradley DM, Clarke AJ. Newborn screening for Duchenne muscular dystrophy. Arch Dis Child 2003;88:91-2.
Mendell JR, Shilling C, Leslie ND, Flanigan KM, al-Dahhak R, Gastier-Foster J, et al.
Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol 2012;71:304-13.
Moat SJ, Bradley DM, Salmon R, Clarke A, Hartley L. Newborn bloodspot screening for Duchenne muscular dystrophy: 21 years experience in Wales (UK). Eur J Hum Genet 2013;21:1049-53.
Das S, Sarala D. Diagnosis of muscular dystrophies: The changing concepts. Neurol India 1998;46:165-76.
Canet E, Praud JP, Bureau M. Chest wall diseases and dysfunction in children. In: Chernick V, Boat T, editors. Kendig's Disorders of the Respiratory Tract in Children. 6th
ed. Philadelphia: Saunders; 1998. p. 787-815.
Nigro G, Comi LI, Politano L, Bain RJ. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiol 1990;26:271-7.
Malik. Heart rate variability: Standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 1996;93:1043-65.
Abhishekh HA, Nisarga P, Kisan R, Meghana A, Chandran S, Raju T, et al.
Influence of age and gender on autonomic regulation of heart. J Clin Monit Comput 2013;27:259-64.
Meghana A, Sriranjini SJ, Sathyaprabha T, Sanjib S, Prathyusha V, Satishchandra P, et al.
Autonomic function in reflex and non-reflex epilepsy – An exploratory study. Acta Neurol Scand 2016;133:459-65.
Udupa K, Sathyaprabha TN, Thirthalli J, Kishore KR, Lavekar GS, Raju TR, et al.
Alteration of cardiac autonomic functions in patients with major depression: A study using heart rate variability measures. J Affect Disord 2007;100:137-41.
Dhargave P, Nalini A, Abhishekh HA, Meghana A, Nagarathna R, Raju TR, et al.
Assessment of cardiac autonomic function in patients with Duchenne muscular dystrophy using short term heart rate variability measures. Eur J Paediatr Neurol 2014;18:317-20.
Sandercock GR, Bromley PD, Brodie DA. Effects of exercise on heart rate variability: Inferences from meta-analysis. Med Sci Sports Exerc 2005;37:433-9.
Telles S, Sharma SK, Balkrishna A. Blood pressure and heart rate variability during yoga-based alternate nostril breathing practice and breath awareness. Med Sci Monit Basic Res 2014;20:184-93.
Raghuraj P, Ramakrishnan AG, Nagendra HR, Telles S. Effect of two selected yogic breathing techniques of heart rate variability. Indian J Physiol Pharmacol 1998;42:467-72.
Vempati RP, Telles S. Yoga-based guided relaxation reduces sympathetic activity judged from baseline levels. Psychol Rep 2002;90:487-94.
Patil SG, Mullur LM, Khodnapur JP, Dhanakshirur GB, Aithala MR. Effect of yoga on short-term heart rate variability measure as a stress index in subjunior cyclists: A pilot study. Indian J Physiol Pharmacol 2013;57:153-8.
Pal GK. Yoga and heart rate variability. Int J Clin Exp Physiol 2015;2:2-9. [Full text]
Grange RW, Call JA. Recommendations to define exercise prescription for Duchenne muscular dystrophy. Exerc Sport Sci Rev 2007;35:12-7.
Jansen M, van Alfen N, Geurts AC, de Groot IJ. Assisted bicycle training delays functional deterioration in boys with Duchenne muscular dystrophy: The randomized controlled trial “no use is disuse”. Neurorehabil Neural Repair 2013;27:816-27.
Routledge FS, Campbell TS, McFetridge-Durdle JA, Bacon SL. Improvements in heart rate variability with exercise therapy. Can J Cardiol 2010;26:303-12.
Muralikrishnan K, Balakrishnan B, Balasubramanian K, Visnegarawla F. Measurement of the effect of Isha yoga on cardiac autonomic nervous system using short-term heart rate variability. J Ayurveda Integr Med 2012;3:91-6. [Full text]
Krishna BH, Pal P, Pal GK, Balachander J, Jayasettiaseelon E, Sreekanth Y, et al.
Effect of yoga therapy on heart rate, blood pressure and cardiac autonomic function in heart failure. J Clin Diagn Res 2014;8:14-6.
Oliveira NL, Ribeiro F, Alves AJ, Teixeira M, Miranda F, Oliveira J, et al.
Heart rate variability in myocardial infarction patients: Effects of exercise training. Rev Port Cardiol 2013;32:687-700.
Telles S, Singh N, Balkrishna A. Heart rate variability changes during high frequency yoga breathing and breath awareness. Biopsychosoc Med 2011;5:4.
Talakad N Sathyaprabha
Department of Neurophysiology, National Institute of Mental Health and Neurosciences, Hosur Road, Bengaluru - 560 029, Karnataka
Source of Support: None, Conflict of Interest: None
[Table 1], [Table 2], [Table 3], [Table 4]
| Article Access Statistics|
| Viewed||1984 |
| Printed||59 |
| Emailed||0 |
| PDF Downloaded||3 |
| Comments ||[Add] |