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Table of Contents
ORIGINAL ARTICLES
Year : 2022  |  Volume : 5  |  Issue : 1  |  Page : 55-64

Comparison of yoga and physiotherapy on motor neuropsychiatric symptoms and quality of life in Parkinson’s disease


1 Department of Physiotherapy, Manipal College of Health Professions, Manipal Hospital, Bangalore campus, Manipal Academy of Higher Education, Manipal, India
2 Department of Physiotherapy, Manipal College of Health Professions, Manipal Hospital, Bangalore campus, Manipal Academy of Higher Education, Manipal, India; KMCH College of Physiotherapy, Kovai Medical Center Research and Educational Trust, Coimbatore, India

Date of Submission05-Dec-2021
Date of Decision23-Jan-2022
Date of Acceptance09-Feb-2022
Date of Web Publication25-Apr-2022

Correspondence Address:
Dr. Suruliraj Karthikbabu
Adjunct faculty, Department of Physiotherapy, Manipal College of Health Professions, Manipal Hospital, Bangalore campus, Manipal Academy of Higher Education, Manipal
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/AOMD.AOMD_49_21

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  Abstract 

Background: Motor and neuropsychiatric symptoms are the manifestations of Parkinson’s disease (PD), leading to poor quality of life of patients. Aim: This study aims to compare the benefits of yoga versus physiotherapy on motor and neuropsychiatric symptoms and health-related quality of life in patients with PD. Materials and Methods: Twenty-four patients with PD, Hoehn and Yahr disease severity rating scale of I–III, score of <3 on a pull test, and walking ability for 10 meters participated in this observer-blinded randomized clinical trial. The yoga group practiced asanas (postures), pranayama (breathing), and meditation. The comparator group underwent physiotherapy. All participants performed 60-minute training sessions a day, with two sessions per week for 12 weeks. The Parkinson’s Disease Questionnaire-39 (PDQ-39), Addenbrooke Cognitive Examination (ACE-R), Beck’s Depression Inventory (BDI), Unified Parkinson’s Disease Rating Scale (UPDRS) motor experiences, and Balance Evaluation System Test (BESTest) were the outcome measurements. Results: On comparing the groups using the Mann–Whitney U test, a statistical significance was observed in the overall quality of life (p = 0.008), emotional well-being (p = 0.008), and stigma (p = 0.048) domains of PDQ-39 and the memory (p = 0.025) and fluency (p = 0.003) domains of ACE-R, which were favorable for yoga. The BDI, UPDRS motor experiences, and BESTest measures were statistically significant (p < 0.05) for both the yoga and physiotherapy groups, only on within-group analysis. Conclusion: Psycho-spiritual yoga practice appears to promote emotional well-being and alleviate the stigma attached to PD; therefore, it improves the quality of life of PD patients compared to physical exercises. In addition, it is noted that patients taking antidepressants may experience less depressive symptoms, warranting a multi-arm parallel-group randomized trial. In conclusion, both yoga and physiotherapy appear to exhibit therapeutic potential in alleviating the motor and neuropsychiatric symptoms of PD and enhancing the balance performance in patients.

Keywords: Cognition, motor skills, Parkinson’s disease, physiotherapy, quality of life, yoga


How to cite this article:
Thunga AV, Karthikbabu S, Prem V. Comparison of yoga and physiotherapy on motor neuropsychiatric symptoms and quality of life in Parkinson’s disease. Ann Mov Disord 2022;5:55-64

How to cite this URL:
Thunga AV, Karthikbabu S, Prem V. Comparison of yoga and physiotherapy on motor neuropsychiatric symptoms and quality of life in Parkinson’s disease. Ann Mov Disord [serial online] 2022 [cited 2022 May 16];5:55-64. Available from: https://www.aomd.in/text.asp?2022/5/1/55/343844




  Introduction Top


Parkinson’s disease (PD) is one of the most common neurodegenerative disorders, affecting approximately 0.3% of the world population, i.e., 10 million people worldwide.[1] The accretion of α-synuclein elements and depletion of dopamine-secreting cells in the substantia nigra causes worsening of the disease with time.[2],[3] The cardinal motor features of PD are hypokinesia, axial and limb rigidity, tremor, and postural instability.[3] In addition to these motor symptoms, postural fatigue and axial motor impairments contribute to the forward flexed truncal posture in patients.[4] The neuropsychiatric features attributed to PD are cognitive decline, apathy, depression, anxiety, fatigue, and sleep disturbances.[5] The loss of postural control and movement dysfunction in patients is associated with a decline in comprehension and emotional status.[6] Anxiety and the fear of falling affect freezing of gait.[7] Motor features and neuropsychiatric symptoms are the key determinants of quality of life.[8],[9] Furthermore, physiotherapy and complementary therapies are recommended for PD patients.[10],[11] Existing rehabilitation strategies for PD patients mainly focus on motor symptoms and physical function. Mak et al.[12] demonstrated that physiotherapy exercises have long-term benefits on balance and mobility. Cueing and dual-task training that require cognitive (mind) and motor skills (body) had a positive influence on balance and gait.[13],[14] A recent meta-analysis concluded that physiotherapy exercises for patients with PD are beneficial in improving motor symptoms, functional balance, mobility, and quality of life.[11]

Psychological distress such as depression and anxiety are prevailing consequences of restlessness and irritation among patients with PD, owing to their dependency on others to meet their daily needs. Psychological distress and severity of motor features are major factors that are positively related to health-related quality of life in patients with PD.[15] They experience psychological distress because of progressive motor dysfunction, difficulty in fulfilling their familial and social roles, and unattended emotional needs. Psychologically informed behavioral strategies may assist patients in accepting and adjusting to living with PD.[16] The Southeast Asian population with mild-to-moderate PD experienced considerable symptom burden and unmet psychosocial, spiritual, and emotional support[17]; this highlights the need to adopt an integrative approach for PD rehabilitation. Yoga is one of the psycho-spiritual complementary therapies that focuses on the interaction between the mind, body, and behavior.[18]

Yoga is a mind–body practice including asanas (postures), pranayama (breathing techniques), dhyana (meditation), and relaxation techniques. During yoga, an individual’s mind is motivated to concentrate on the proprioception and awareness of the body.[18] In addition, yoga promotes general body relaxation, as well as the mental and emotional well-being of an individual. Although previous trials have yielded promising results of the efficacy of yoga[19],[20],[21],[22],[23],[24] on motor function, they viewed yoga as a form of exercise rather than a holistic approach. A recent systematic review recommended that more trials are required with optimal dosage and specific interventional protocols designed for patients with PD.[25] In a systematic review, Kwok et al.[26] reported the benefits of mind–body exercises on motor features, balance, and functional mobility for patients with PD. However, the therapeutic potential of yoga on psychosocial well-being in PD are understudied, warranting disease severity-specific psycho-spiritual yoga modules. The aim of this study was to compare the benefits of yoga versus physiotherapy on motor and neuropsychiatric symptoms and assess their effect on the quality of life of patients with PD. We hypothesized that compared to physiotherapy, yoga may result in improvements for multiple outcomes in PD.


  Materials and Methods Top


The study protocol was approved by the Institutional Research Committee of Manipal College of Health Professions, Manipal. The approval was reviewed and consented by the research committee of Manipal hospital, Bangalore. The study was conducted in accordance to the declaration of Helsinki. Our study was registered in the clinical trial registry of India (http://www.ctri.nic.in/): CTRI/2019/06/019618. The trial followed the CONSORT guidelines and its extension to nonpharmacological interventions.

In this assessor-blinded randomized clinical trial, the patients with PD from the neurorehabilitation unit of Manipal hospital, Nightingales Acting Ageing Centre, Amrita Physiotherapy and Pain Relief Clinic, and local yoga centres were recruited through convenience sampling between May 2019 and March 2020. The neurologists diagnosed PD using the Queen’s Square Brain Bank criteria. The patients in the yoga and physiotherapy groups were advised to continue antiparkinsonian medications such as 300-mg levodopa per day as recommended by the neurologist. Other nonpharmacological interventions were withheld throughout the study period. Patients with Hoehn and Yahr PD severity rating of I–III, ability to understand and follow simple verbal instructions, score of <3 on a pull test, and independent walking ability for 10 meters were included in the study. The exclusion criteria included Parkinson’s plus syndrome, vascular  Parkinsonism More Details, other neuromuscular diseases, Alzheimer’s disease, severe auditory and visual deficit, and recent deep brain stimulation or pallidotomy.

The objective and methods of the trial were explained to the patients. Initially, a patient information sheet was provided to them explaining the interventions that were formulated specific to their problems. Their capacity to perform the exercises was gauged. Written consent was then obtained from the eligible patients. The patients were randomly assigned to the two interventional groups, yoga and physiotherapy, through block randomization. A block size of four was prepared with an allocation ratio of 1:1; a total six blocks were prepared. An independent research coordinator generated the allocation details of the training arms in sequentially numbered opaque sealed envelopes. A physiotherapist who was also qualified in neurosciences conducted the study intervention. Two qualified physiotherapists with 2 years of clinical experience who were blinded to the allocation collected all the outcome measures.

Interventions

The yoga group practiced six basic asanas, pranayama, meditation, and relaxation. This training module was designed by experts utilizing the principles of yoga. The asanas were administered considering the patients’ abilities and movement limitations. Props such as bricks, belts, and ropes were introduced initially and used until the participants could perform the postures without them. The asanas were modified for each stage of the Hoehn and Yahr scale. The patients performed individualized asanas under the supervision and assistance of the therapist. The asanas included were Ardha Kati Chakrasana (lateral arc posture), Setubandhasana (bridge posture), Suptaudarakarshanasana (folded leg posture), Ardhapavanamuktasana (half wind releasing posture), Bhujangasana (serpent posture), Ardha Shalabhasana (half locust posture), and Shavasana (deep relaxation technique) [Figure 1]. The asanas and steps to practice them are presented in Appendix-A. The patients executed Vibhagya (abdominal, thoracic, and shoulder) and Bhramari pranayama, followed by meditation (Nandanusandhana and Om dhyana). They were instructed to perform the program at home on the remaining days. Each yoga session lasted for 60 minutes, and two sessions were conducted each week for 12 weeks [Table 1].
Figure 1: Yoga asanas. A-Ardha Kati Chakrasana; B- Setubandhasana; C- Ardhapavanamuktasana; D- Suptaudarakarshanasana; E, F- Bhujangasana; G- Ardha Shalabhasana; H- Shavasana

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Table 1: The dosage of yoga asanas, pranayama, and meditation

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The physiotherapy group received movement and balance-specific exercises. The patients performed breathing exercises, lower limb strengthening, trunk rotations, bridging, sit-to-stand, cat–camel, arm reach-outs in a quadruped position, balance exercises, and mobility exercises. Participants performed catching and throwing a ball in the seated position [Figure 2]. The balance exercises were initially performed while standing with a wide base of support and then with the feet placed together. The patients performed single-leg standing, heel raises, and partial wall squats, with and without the therapist’s support. The exercises then progressed to tandem standing, standing on unstable surfaces such as a foam pad and wobble board, side walking, and obstacle course gait training. Each physiotherapy session lasted for 60 minutes twice a week for 12 weeks.
Figure 2: Physiotherapy exercises. A- Bridge; B, C- Cat and camel exercise; D- Strengthening exercise; E- Sit-to-stand; F- Throwing and catching a ball; G- Arm reach-outs

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Outcome measures

The outcome measurements were as follows: Parkinson’s Disease Questionnaire-39 (PDQ-39), Addenbrooke Cognitive Examination (ACE-R), Beck’s Depression Inventory (BDI), motor experiences of the Unified Parkinson’s Disease Rating Scale (UPDRS), and Balance Evaluation System Test (BESTest). PDQ-39 is a self-reported questionnaire form that assesses how often patients with PD have trouble across various dimensions of function such as mobility, daily activities, bodily discomfort, social support, stigma, communication, and cognitive and emotional well-being. The test–retest reliability of PDQ-39 was 0.76–0.93 with a Cronbach’s alpha value of 0.72–0.95.[27] The ACE-R recognizes and distinguishes the cognitive decline of patients with PD. This tool consists of 19 cognitive tasks including attention, memory, fluency, language, and visuospatial functioning. The total ACE-R score and verbal fluency subscore had a specificity of 0.87 and sensitivity of 0.70 and 0.92, respectively, in differentiating PD from progressive supranuclear palsy.[28] BDI evaluates the attitudes and symptoms of depression and interprets the level of depression among patients with PD. BDI is a reliable and responsive tool to examine the status of depression in PD.[29] UPDRS part-III examines the motor features of speech, facial expression, rest and action tremor, rigidity, fingers and hand movement, leg agility, postural stability, sit-to-stand, posture, and gait. Test–retest reliability for the motor subscale of UDRS was high with an intraclass correlation coefficient (ICC) of 0.90.[30] BESTest is a 5-point ordinal scale that assesses the balance capacity under the following six domains: biomechanical constrictions, limits of stability, anticipatory and reactive postural responses, orientation of sensory systems, and dynamic balance while walking. The test–retest reliability (ICC ≥ 0.88) and interrater reliability (ICC ≥ 0.91) for BESTest were high.[31] BESTest showed a sensitivity of 0.84 and specificity of 0.76 for detecting PD fallers from non-fallers.[31]

Data analysis

Data were analyzed using the SPSS version 16.0 software (IBM for Windows, SPSS, Illinois, USA). The continuous and nominal variables of the yoga and physiotherapy groups at baseline were compared using a t-test and chi-squared test. The sample size of our study was 24 (12 patients per group). As a result, the statistical power to perform bivariate analysis and the normal distribution of 12 cases in each group was not adequate and the homogeneity of variance were uncertain. Therefore, we used the Mann–Whitney U test, which is the nonparametric alternative to the independent t-test, to analyze the differences in the outcome measures between the two groups. A Wilcoxon signed-rank test was conducted to analyze the within-group change in the outcome measures. A p value of <0.05 was considered to be statistically significant. The analysis had a total of 50 multiple comparisons for the outcome measures. The false discovery rate, a correction for multiple comparisons, was employed to minimize a type-1 error. The DATA LIST free/p (F5.3) command was used in the SPSS software to create a dataset having the p values of all multiple tests (data lines between BEGIN DATA and END DATA, with the list of p values in the descending order).


  Results Top


Out of 40 individuals that were screened, 24 were enrolled in the study. After randomization, 12 patients were assigned to each group. Patients from both groups completed 12 weeks of their respective intervention programs and were considered for analysis. Although some patients experienced discomfort during the initial 2 weeks, none of them reported any adverse symptoms during and after the yoga practice and physiotherapy training. [Figure 3] describes the CONSORT flowchart. The demographic characteristics and clinical measures of the patients at baseline are listed in [Table 2]. All the baseline variables between the yoga and physiotherapy groups showed no statistical significance except for BDI (p = 0.015; [Table 2]).
Figure 3: CONSORT flow diagram

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Table 2: Demographics and clinical variables at the baseline*

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A statistical significance was observed for the PDQ-39 (p = 0.008), emotional well-being (p = 0.008), and stigma (p = 0.048) domains of PDQ-39 when comparing the yoga and physiotherapy groups, which were favorable for yoga. Posttraining, the memory (p = 0.025) and fluency (p = 0.003) domains of ACE-R showed a statistical difference between both groups. BDI was not statistically significant (p = 0.186) for the groups. However, the within-group analysis revealed a statistical improvement for the yoga and physiotherapy groups (p < 0.05). Similarly, the motor experience of UPDRS (p = 0.617) and BESTest (p = 0.105) was not statistical significant when compared between the groups but was statistically significant for the within-group analysis. [Table 3] shows the within-group and between-group changes in the outcome measures. After correction with the false discovery rate, 23 tests showed statistically significant = results (variable test = 1) [Table 3].
Table 3: Within-group and between-group changes in the outcome measures

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This preliminary data of PDQ-39 showed a mean difference (standard deviation) of 9.75 (7.84) for the yoga group and 2.47 (3.2) for the physiotherapy group. Given the effect size (d = 1.22), 5% level of significance and 80% power, a priori sample size was calculated using the GPower 3.1 software package. According to this calculation, the required sample size for each intervention arm is 19 subjects. To report statistical significance between yoga and physiotherapy, future trials should recruit a total sample size of 42 individuals considering a 10% dropout rate.


  Discussion Top


The objective of the current study was to investigate the effects of yoga versus physiotherapy on neuropsychiatric symptoms and quality of life in patients with PD. The superior effects of yoga as observed with the PDQ-39 questionnaire and on emotional wellbeing can potentially be mediated by spiritual resilience. The emotional distress experienced with anxiety and depression affects spiritual resilience, which, in turn, affects the quality of life.[32] Patients with PD who exhibit high emotional distress tend to experience low spiritual resilience and poor quality of life. The indicators of spiritual resilience such as the levels of perceived affliction and equanimity partially mediate the relationship between emotional distress (anxiety and depression) and quality of life.[33] This suggests that since yoga is a mind–body–spirit model, it may help in alleviating psychological distress. Furthermore, it may enable patients to accept and adjust to their daily living activities and illness with better emotional stability; therefore, it enables them to have a meaningful health-related quality of life.[16] This finding is supported by Kwok et al.[34] who showed the therapeutic benefits of psycho-spiritual-based yoga training over physical exercises in reducing the symptoms of anxiety and depression in patients with PD. The potential drawback of our study is that the aspect of anxiety and spiritual resilience was not evaluated. The benefits of psycho-spiritual-based yoga on spiritual resilience (perceived affliction and perceived equanimity) with a holistic well-being scale should be investigated in future studies.

Yoga and exercise are believed to alleviate depression by enhancing the balance of monoamines (dopamine, serotonin, and noradrenaline), regulating the hypothalamic-pituitary-adrenal axis function, and improving the levels of β-endorphin.[35] Activation of the parasympathetic nervous system and prefrontal cortex subregions that control the allostatic load with yoga may reduce the level of depression our study patients.[36] A systematic review by Jin et al.[25] concluded that yoga can reduce the symptoms of depression in patients with PD and improve their motor function and quality of life. Yoga asanas involving large amplitude movement, pranayama, and mindfulness elements may directly facilitate the vagal efferent system and the basal ganglia and cerebellar circuits, with corresponding increased autonomic, emotional, and cognitive regulation.[35] Future studies should confirm the therapeutic potential of yoga on the abovementioned neurophysiological and neurocognitive mechanisms. Cognitive dysfunction in PD, in particular, attention-deficit disorders, severely affects the quality of life.[37] The execution of asanas, pranayama, meditation, and relaxation (Shavasana) requires regular feedback, attention, and concentration; this cognitive improvement was clearly reflected in the ACE-R score.[38] Furthermore, auditory cueing and skills with yoga that focused on perception and awareness may have contributed to these cognitive changes.[39] A systematic review by Leung et al.[40] reported that as a cognitive training strategy, cueing helps in improving cognition. In addition, yoga appears to alleviate the stigma attached to PD, warranting further research in this area. Ma et al.[41] identified that in patients with PD, the stigma of the illness was a critical factor influencing their health-related quality of life.

The changes in the motor experience of the UPDRS and BESTest scores could be related to the effects of yoga and physiotherapy, as well as the training dosage. Yoga is usually performed in a slow, rhythmic, and coordinated movement pattern with breath control.[42] Longer duration and higher dosage of physical exercises are necessary for the reduction in PD motor symptoms[43] and improvement in balance and mobility.[44] The consistent 12 weeks of yoga and physiotherapy sessions (24 supervised sessions) in our study may have affected the patients’ muscle tone, muscle power, muscular coordination, posture, balance, and mobility. Yoga postures, in particular, Bhujangasana and Shalabhasana, performed in the prone position are known to strengthen the back extensors; therefore, patients have better trunk control and postural biomechanical alignment.[45] In addition, yoga postures and physiotherapy exercises may enhance the body’s awareness and sense of balance, promoting self-efficacy in patients with PD through the facilitation of vestibular and proprioceptive sensory inputs.[46] Yoga asanas and physiotherapy exercises involve dynamic weight shifts of body posture and movements towards the limits of balance stability, which habitually demand anticipatory and reactive postural control.

Despite these promising findings, our study has some limitations. Our trial included only 24 participants with no follow-up. We were unable to recruit the required sample size because of the time-bound nature of the study and the unprecedented lockdown owing to the ongoing coronavirus disease 19 pandemic. Furthermore, there was heterogeneity of the study population with regards to the disease severity grading. Moreover, in the absence of follow-up examination, it is difficult to understand whether the emotional well-being demonstrated by the participants was maintained over time. Despite weekly telephonic calls to the patients to inquire about their consistency with the training exercises, their compliance at home was not ensured and documented. A major limitation of this study is that we did not collect the full profile of the medications taken by the patients. Considering the progressive nature of the disease, the dose and dosage of yoga and physiotherapy training required for patients with PD is of a higher intensity; however, the intensity of training was moderate in our study. Since the motor and neuropsychiatric elements are both affected in PD, healthcare professionals should consider a holistic approach to mind–body interventions. Future PD trials should consider including yoga with physical therapy for multiple beneficial outcomes. In particular, anxiety is an important symptom worth investigating in psycho-spiritual yoga studies.

Psycho-spiritual yoga practice appears to promote the emotional well-being of patients and alleviate the stigma attached to PD, in turn, remarkably improving the quality of life compared to physical exercises. However, patients on antidepressants may experience milder depressive symptoms, warranting a multiarm parallel-group randomized trial. In conclusion, yoga and physiotherapy both have therapeutic potential in alleviating the motor and neuropsychiatric symptoms of PD and enhancing balance performance.

Acknowledgements

We are grateful to study participants for their voluntary contribution. We extend our gratitude to Nightingales Acting Ageing Centre, Amrita Physiotherapy & Pain Relief Clinic, and Manipal hospital, Bangalore and MCHP, MAHE.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Author contribution

Akash V Tunga: Concept (yoga), Investigation, Data curation, Project administration, Reviewing and Editing. Suruliraj Karthikbabu: Study concept and specifying research question, Methodology, Formal analysis, Writing the manuscript, Venkatesan Prem: Concept (yoga), Supervision, Visualization, Reviewing and Editing.

Ethical compliance statement

The study was conducted in accordance to the declaration of Helsinki.

Clinical Trial registration

http://www.ctri.nic.in/ [CTRI/2019/06/019618], registered prospectively in Clinical Trial Registry of India.

Data availability

The information can be obtained from the author on request

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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