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Table of Contents    
REVIEW ARTICLE
Year : 2021  |  Volume : 69  |  Issue : 5  |  Page : 1165-1175

The Rationale of Yoga in Parkinson's Disease: A Critical Review


1 Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
2 Department of Psychiatry, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
3 Department of Biostatistics, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India

Date of Submission21-Aug-2020
Date of Decision19-Dec-2020
Date of Acceptance17-Jan-2021
Date of Web Publication30-Oct-2021

Correspondence Address:
Pramod Kumar Pal
Professor, Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Hosur Road, Bengaluru - 560 029, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.329545

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 » Abstract 


Background: Patients with Parkinson's disease (PD) commonly use complementary and alternative medications. Yoga is a mind-body intervention that is being increasingly explored as a tool in the therapeutic armamentarium of PD.
Objective: To critically evaluate the studies and summarize the utility of Yoga in PD.
Material and Methods: We performed a systematic literature search in the Medline and Cochrane databases and included randomized controlled trials (RCT) of Yoga in PD. The studies were evaluated for internal validity and the relevant data were extracted.
Results: A total of seven studies were included in the analysis. We collated the data on the changes in motor function, gait and balance parameters, anxiety, depression and quality of life scores observed after intervention (Yoga) in patients with PD and highlighted the limitations of these studies.
Conclusion: Anxiety, depression, and balance issues in PD may benefit from Yoga. Yoga has potential as an add-on therapy in PD.


Keywords: Parkinson's disease, systematic review, Yoga
Key Message: Yoga is a mind body exercise, cost effective and non-invasive. Anxiety, depression and balance issues in Parkinson 's disease (PD) may be benefited by Yoga. Yoga has potential as an add-on therapy in PD.


How to cite this article:
Mailankody P, Varambally S, Thennarasu K, Pal PK. The Rationale of Yoga in Parkinson's Disease: A Critical Review. Neurol India 2021;69:1165-75

How to cite this URL:
Mailankody P, Varambally S, Thennarasu K, Pal PK. The Rationale of Yoga in Parkinson's Disease: A Critical Review. Neurol India [serial online] 2021 [cited 2021 Dec 3];69:1165-75. Available from: https://www.neurologyindia.com/text.asp?2021/69/5/1165/329545


Parkinson's disease (PD) is a neurodegenerative disease characterized by progressive loss of dopaminergic neurons leading to asymmetric tremor, bradykinesia, rigidity, and postural imbalance.[1] Also, patients with PD can have anxiety, depression, anosmia, constipation, sleep disturbances, sensory symptoms, memory loss, and autonomic dysfunction.[2] In addition to dopamine, there can be a disruption in the homeostasis of other neurotransmitters like serotonin, glutamate, noradrenaline, and acetylcholine in PD.[1] In patients with PD, the standard treatments for depression are not very effective. A meta-analysis evaluating the efficacy of antidepressants in PD showed that the efficacy of the overall pharmacological interventions was not significant (P = 0.054).[3]

Yoga is a mind-body practice wherein movements, postures, and breathing practices are utilized to achieve optimum relaxation.[4] Yoga-based interventions have been used as a therapeutic tool in several neurological, psychiatric, and other medical illnesses.[4] As stated above, PD is a disease characterized by motor, cognitive, autonomic, and behavioral issues. Yoga, with its beneficial effect on all these domains, has the potential to be a useful tool in the therapeutic armamentarium of PD. A survey on the use of complementary therapy in PD found that 84 among the 272 respondents performed Yoga, and more than 70% found it to be effective.[5] Several studies and meta-analysis have evaluated the benefits of Yoga in PD.[6],[7],[8],[9],[10],[11],[12],[13] Our objective is to critically evaluate the studies and summarize the effect and rationale of Yoga as a therapeutic tool in PD.


 » Methods Top


Search strategy

We followed the pertinent criteria of the preferred reporting items for systematic reviews and meta-analyses (PRISMA) [Figure 1]. We searched the literature published in Medline and Cochrane databases till May 2020 following keywords “[Parkinson's disease] OR [Parkinson disease] OR [Parkinson's disease] AND Yoga. The cross-references from the articles were also screened. Some of the studies, which were not relevant to the article, were excluded after screening the titles, abstracts, or full texts of articles obtained from the database.
Figure 1: Flowchart of study selection

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Study selection

Studies were considered for analysis if: (1) they were Randomized controlled trials (RCT) (2) full text was available in English. Only Randomized controlled trials with human subjects with PD were included for the study [Table 1]. Review articles, studies on PD which did not include Yoga, conference abstracts with no full texts were excluded from the review.
Table 1: Summary of Trials

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Data extraction and study quality assessment

The following data were extracted from the included studies: Name of the first author, the country, the year of study, the number of participants, the type of intervention received, outcomes of the study, results, and limitations. Two researchers [PM and KT] independently evaluated each of these studies for internal validity[14] [Table 2] and sorted out disagreements by discussion and mutual agreement. We have tabulated a summary of the evidence available for Yoga in each of the domains in PD [Table 3].
Table 2: Internal validity of the studies*

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Table 3: Evidence for Yoga in PD: A summary

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 » Results Top


The details of the trials, the outcome measures, and the results are summarized in [Table 1]. Five among the seven studies (71.4%) were Class II [Table 2]. The studies by Ni and Myers (28.6%) used Vinyasa Yoga, and the remaining five studies used Hatha Yoga as the intervention modality. Only patients who were ambulant and could walk unaided were recruited in these studies. Patients with Hoehn and Yahr (H and Y) stage more than 3 [more severe] were not included in any of the studies. It would be expected that Yoga would be studied extensively in the country of its origin, India. Surprisingly, all the studies except one were carried out in the United States of America. Though many studies have been carried out in the field of Yoga, studies of Yoga in patients with PD are lacking from the Indian subcontinent.

Motor scores were assessed in all seven studies. However, the studies assessing other parameters like depression, anxiety, and cognition are limited in number. Only one study evaluated anxiety,[8] two studies (28.6%) evaluated depression,[8],[12] five studies (71.4%) evaluated balance.[7],[9],[11],[13],[15]

Colgrove et al. reported the changes in physiological measures like blood pressure and pulmonary function tests in the study in another paper published three years after the first paper.[9],[16] Quality of life, fatigue, activity constraints, balance confidence and ability to control falls were analyzed and published in a separate paper by Puymbroeck et al.[7],[17] Ni et al. analyzed bradykinesia, rigidity, muscle strength and power in comparison with the control group and reported them in a separate publication.[10],[15]


 » Discussion Top


Effect of Yoga on motor scores

Eight weeks of yoga practice resulted in an improvement in the mean Unified Parkinson's Disease Rating Scale (UPDRS) III scores by 5.2 [95% CI -8.2 to -2.2] and 6.4 [SD; 8.3] in the two recent RCTs by Kwok et al. and Puymbroeck et al. respectively.[7],[8] A change of 4.5 to 6.7 points of UPDRS motor score was considered to be of moderate clinically important difference by Shulman et al.[18] A change in 5 points in the UPDRS motor score was considered as clinically meaningful change by Schrag et al.[19] An elegant network analysis by Zhuo et al. found a mean UPDRS III difference of -6.05 (-12.06, -0.04) for Levodopa, -3.86 (-5.87, -1.86) for Pramipexole, -5.05 (-5.95, -4.15) for Ropinirole, -3.85 (-5.89, -1.81) for Selegiline when compared with placebo.[20] So, in terms of UPDRS III, the improvement achieved with Yoga is significant and clinically meaningful, though direct comparison with pharmacotherapy may not be feasible with the current evidence.[8],[13]

In a secondary analysis by Ni et al., patients with PD who underwent Yoga intervention had statistically significant improvement in bradykinesia and rigidity assessed by UPDRS as compared to the control group. The same group evaluated the strength and power of different muscle groups with pneumatic resistance machines. The Yoga group was found to have a significant improvement in strength as compared to the control group. However, the improvement in power was not significant, except for the leg press.[10]

Effect of Yoga on balance, postural stability, freezing of gait and falls

The incidence of falls in PD is as high as 68% in PD.[21] The pharmacological options available at present for addressing the postural stability, balance, and falls in PD are not satisfactory.[22],[23] A systematic review and meta-analysis revealed a significant improvement in postural stability, gait, freezing, and falls in PD after Deep brain stimulation (DBS) of the pedunculopontine nucleus (PPN). However, the improvement was not sustained beyond a year.[24] Subthalamic nucleus DBS also produces significant improvement in gait and freezing in patients with PD.[25]

Several studies of Yoga in PD show a significant improvement of balance with Yoga.[7],[11],[15] The RCT by Myers et al. found that the patients with PD were more stable and erect after 12 weeks of Yoga and had a quick and appropriate response to external stimuli. Transition, anticipatory movements, verticality balance, and sensory orientation were significantly better after Yoga. The study by Myers is the only study that evaluated the effect of Yoga on the various components of balance (BESTest) in patients with PD.[11] The randomized wait-list controlled pilot study by Puymbroeck et al. also addressed balance issues and was designed to determine changes in motor function, functional gait, postural stability, and balance control for community-dwelling individuals with PD. In addition to improvement in motor function and postural stability, the patients in the Yoga group experienced a significant reduction in freezing of gait and risk of falls.[7] Though the balance confidence and the belief in the ability to manage falls showed a significant improvement in the patient group, the belief in the ability to control and prevent falls did not significantly improve in the patient group or the control group.[17] The balance was assessed with the help of the Berg Balance Scale (BBS) by Colgrove et al. When the results were analyzed by removing two participants who showed ceiling effect, the improvement was statistically significant. Nevertheless, the overall result failed to show significance.[9] Falling episodes declined by 25% in the yoga group in the same study.[16] An elegant review by Sumec et al. described the interconnection between balance and anxiety. The improvement in balance by itself could lead to an improvement in anxiety.[26]

According to the meta-analysis of the various mind-body interventions in PD by Kwok et al., the improvement in balance and postural stability achieved with Yoga is comparable to that of dance and Tai Chi. However, the improvement in motor scores was much better with Yoga therapy than Dance therapy or Tai Chi.[6]

Effect of Yoga on non-motor symptoms

Effect of Yoga on anxiety in PD

Kwok et al. noted significant improvement in anxiety in patients with PD after eight weeks of Yoga, which remained significant even during follow up three months after the intervention.[8] In the study by Myers et al., the change in anxiety levels were not significantly different from those of controls in patients who underwent Vinyasa Yoga. However, the baseline anxiety scores were low in most of the patients.[11] Yoga can decrease cortisol levels and increase GABAergic activity, thereby leading to improvement in mood and alleviation of anxiety.[27] In healthy subjects also Integrated Yoga has been found to be superior to exercise for anxiety-related symptoms.[28]

Effect of Yoga on depression in PD

Kwok et al. found that eight weeks of Yoga resulted in significant improvement of depression in PD and the improvement following Yoga was more than the improvement observed after stretching and resistance training exercise.[8] A significant improvement in the depression scores was also found in some other studies with pre-test post-test design.[29],[30]

Yoga and quality of life in PD

The quality of life, as assessed by Parkinson's disease questionnaire 8 (PDQ8), was better after Yoga as compared to stretching and resistance training exercise. The Yoga group performed better than the exercise group in terms of holistic well-being as assessed by the holistic well-being scale. The perceived hardship features like emotional vulnerability, spiritual disorientation, and bodily irritability significantly decreased in the patients who underwent Yoga therapy. The characteristics of perceived equanimity like nonattachment, mindful awareness, general vitality, and spiritual self-care also improved in these patients.[8] Walter et al. also noted significant improvement of PDQ8 scores in the experimental group, though the difference was not significant across the groups.[17] The improvement in the quality of life as assessed by the PDQ 39 scale was significant for mobility, Activities of daily living, and the sum when compared to the control group.[10] Hawkins et al. also found that Yoga resulted in improved activities and outcomes in participation like mobility, social relationships, self-care, handling stress, recreation, thereby suggesting that the improvement in the quality of life noticed in the scales administered was translated into real life.[31] A recent mixed methods study evaluated the changes in quality of life after merging Yoga practice and Occupational therapy for patients with PD. Though there were no significant changes in the quantitative analysis, the qualitative study found patient-perceived improvement in all aspects of PDQ-8 and authors suggest that social support contributed to this perceived benefit.[32]

Yoga and sleep in PD

There are no RCTs that evaluated the benefit of Yoga for sleep disturbances in PD. However, physical activity can significantly improve sleep efficiency in patients with PD.[33] Yoga has been found to significantly improve sleep quality in a healthy elderly population.[34]

Yoga and cognition in PD

A pilot study by Bega et al. found no cognitive benefit for the Yoga group. However, only one parameter was assessed, and the details of testing were not provided.[13] Although there are no studies done to assess the effect of Yoga on cognition in patients with PD, exercise has been shown to have a beneficial effect on several domains of cognition like mental flexibility, processing speed, and sustained attention.[35] Further, yoga-based intervention has been shown to improve several cognitive domains, sleep measures, and quality of life in elderly subjects with subjective memory complaints.[36],[37]

According to the Movement Disorders Society- Evidence-Based Medicine (MDS EBM) Committee, there were no randomized controlled trials that met their inclusion criteria for the treatment of anxiety disorders, rapid eye movement sleep behavior disorder (RBD), excessive sweating, impaired olfaction, or ophthalmologic dysfunction.[38]

Other benefits of Yoga in PD

Patients with PD had a significant decrease in the perceived constraints as assessed by Activities Constraint scale (ACS) concerning participation in activities, and the change was statistically significant between the patient and control groups.[17] The same study found that fatigue, as assessed by Parkinson's fatigue scale -16 (PFS) improved significantly in patients performing Yoga practice. Nevertheless, the difference was not statistically significant between the patient and the control groups.[17] A significant decrease in low back pain was observed in patients with PD after 12 weeks of Yoga compared to controls.[11] Patients reported an apparent decrease in tremor, more energy, more relaxation, improved sleep, and better mood after Yoga.[16],[39] A few patients noted a reduced 'need' to take the next dose of medication.[16],[40]

Most of the patients enjoyed the sessions and expressed interest to practice Yoga after the study.[11],[12] The patients were found to be continuing Yoga 6 months to 1 year after completion of the trial.[12],[16] However, Bega et al. found that adherence to practice was better in the Resistance training group as compared to the Yoga group.[13]

Comparison of Yoga with other treatment modalities

The utility of Yoga was explored only as an add on therapy in all the trials. So, with the available evidence, a direct head to head comparison of Yoga with pharmacotherapy or DBS may not be possible. The improvement in motor scores is similar for both Yoga and resistance or power training.[8],[15] One class II study demonstrated that Yoga is superior to resistance training for improving anxiety and depression in patients with PD.[8] Improvement in balance may be slightly better with Yoga as compared to power training.[15] A meta-analysis comparing the effect size of different mind body interventions in PD showed that Yoga was superior to Tai Chi in terms of improvement of postural instability and Motor scores.[6] One study found dance to be superior to Yoga and Tai Chi for postural instability in PD.[6] However, apathy, depression, and global cognitive function in PD did not improve with dance therapy.[41]

The quality of evidence is weak for the currently available pharmacotherapy for anxiety and depression in PD.[3],[38],[42] Also, DBS of the STN can lead to several significant adverse effects such as depression and may even lead to suicide.[43] DBS may worsen cognition, especially executive function and verbal fluency.[44],[45]

Given the above, Yoga appears to be a promising tool for the management of balance, anxiety and depression in PD. Yoga has no drug interactions and minimal side effects if done under supervision. It is cost-effective, and medical supervision is not required. These advantages make Yoga an attractive option. However, there is a need for well-conducted controlled clinical trials to establish yoga-based intervention as a defintive treatment option.

The rationale for Yoga as an intervention in PD

Yoga is a combination of physical activity and mindfulness.[46] A meta-analysis by Fang et al. revealed that even moderate exercise significantly reduces the risk of PD.[47] People who habitually exercise had a greater preserved motor and non-motor functions in PD compared to those patients who led sedentary lifestyles. A Raclopride positron emission tomography (PET) study suggested higher dopamine release in patients who did habitual exercise.[48] There are no functional imaging studies done in connection with Yoga and PD.

Both Exercise and Yoga can increase the levels of Brain-Derived Neurotrophic Factor (BDNF), which plays an essential role in the regulation of synaptic plasticity and neurogenesis.[49],[50],[51] A recent review by Li et al. identified that physio exercises lead to the reconstitution of basal ganglia function by increasing the release of BDNF.[52] In an elegant review, Pedersen et al. explained that exercise causes the release of certain substances from the skeletal muscle, which cross the blood-brain barrier and promote the expression and production of BDNF.[53] Pedersen elaborated in detail the various mechanisms by which exercise increases BDNF and substantiates the presence of a muscle brain endocrine loop in this review.[53]

PD, the autonomic nervous system, and Yoga

Orimo et al. reviewed the involvement of the sympathetic and parasympathetic systems in PD. Though both are involved, they conclude that the sympathetic nervous system bears the brunt of PD pathology.[54] Patients with PD also have higher levels of cortisol.[55] The regular practice of Yoga favors a shift from the sympathetic to parasympathetic tone due to the relatively more utilization of type 1 than type 2 muscle fibers.[46],[56] Bowman et al. observed a significant increase in vagal (parasympathetic) activity in healthy elderly persons after Yoga, but not after aerobic exercise.[57] Meditation and breathing practice of Yoga has been held to be responsible for the beneficial effect on cortisol levels and improved parasympathetic activity, rather than the exercise component.[58] The practice of Yoga can increase the vagal tone, improve the parasympathetic scores, and reduce the sympathetic parameters.[59],[60] The practice of Yoga has beneficial effects on heart rate variability.[61] Yoga lowers sympathetic stimulation, decreasing the levels of epinephrine and norepinephrine, unlike aerobic exercise, which increases the sympathetic stimulation.[62],[63]

A nested case-control study found that the long-term use of β2-agonists like Salbutamol was associated with a decreased risk of PD.[64] Hopfner et al., suggested that the beneficial effect of β2-agonists could be mediated by smoking, and β blocker prescription could be triggered by the symptoms of PD, suggesting reverse causation.[65] Nevertheless, another population-based study found that the β agonists and β blockers do not affect the incidence of PD.[66] Mittal et al. elucidated the mechanism by which β receptor controlled the alpha-synuclein gene, thereby influencing the risk of PD.[67] Salbutamol, on long term use, can lead to the downregulation of beta receptors and the development of reduced sensitivity.[68],[69] A decrease in the beta receptor density and decrease in the adenyl cyclase activity are the mechanisms of receptor downregulation.[68] We hypothesize that this downregulation leads to decreased sympathetic activity and an increase in the parasympathetic activity, simulating the effect of Yoga. Yoga, especially the meditative component, has been known to decrease the sympathetic tone and increase the parasympathetic activity.[57] Long term Yoga may hence simulate the effect of Salbutamol and possibly decrease the incidence of PD.

Another recent paper suggests an increase in the incidence of PD in those people with higher socioeconomic status and a decreased incidence in those with lower socioeconomic status.[70] PD mimic flies showed stronger, faster visual responses when they were young. Nevertheless, there was a loss of response in old age.[71] Those people with higher socioeconomic status usually have more demanding jobs, requiring quick responses and decision making, which translates to more frequent sympathetic stimulation and overactivity. Higher incidence of PD in people with more stressful jobs and lower incidence of PD in patients who have used long term salbutamol suggests a role for the sympathetic system. Yoga practice, by countering the effects of sympathetic overactivity and restoring the autonomic balance, could potentially help in decreasing the incidence of PD

Caveats of Yoga as a therapeutic tool

Patients with preclinical PD may have lesser motivation than their healthy counterparts to engage in physical activity, thereby hampering compliance and adherence to Yoga therapy.[72],[73] More than 20% attrition noted in Kwok's study was mostly due to poor motivation and adherence.[8] Cheung et al., in their study, found that sleep, the outlook aspect of quality of life, and physical activity levels were worse in the Yoga group as compared to the control group. However, this pilot study had a wait-list design, and the sample size was small.[12] Different study groups adopt different types and protocols of Yoga, and most studies do not describe the yoga practices used in detail nor any specific tools to assess adverse effects. This heterogeneity limits the replicability and safety of such interventions. The heterogeneity of the study groups and methodology makes it difficult to draw robust conclusions [Table 4]. Nevertheless, standardized and validated protocols have been recently devised for Yoga therapy in PD.[74],[75],[78]
Table 4: Caveats of Yoga as a therapeutic tool

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Future directions

Yoga leads to an increased release of BDNF, has a beneficial effect on the autonomic nervous system and hypothalamic-pituitary (HPA) axis. Telomerase activity, which is an indicator of genomic stability, was found to be higher in Yoga practitioners.[76] Yoga practitioners with a minimum of 2 years of experience were found to have longer telomeres, and lower levels of oxidative markers, homocysteine, malondialdehyde compared to the sedentary healthy general population.[77] Studies evaluating the effect of Yoga on telomere length and oxidative markers in patients with PD will help in a better understanding of the mechanism of action of Yoga in PD.

Head to head comparison of Yoga with other types of physical activity in both healthy subjects and patients with PD need to be carried out. The changes in the scores of tremor, rigidity, and bradykinesia due to Yoga need to be analyzed so that we get a better idea regarding the kind of improvement we can expect after Yoga. The beneficial effects of Yoga require long term practice, and hence trials to administer and evaluate interventions of longer duration need to be designed. As blinding of participants is not possible, better study designs have to be adopted. The incidence of PD and other degenerative diseases in Yoga practitioners need to be compared to the incidence in people who do not practice Yoga to understand whether the benefits of Yoga are translated to real-life with longitudinal studies. Large and longitudinal follow up studies are required to evaluate the potential of Yoga as a prophylactic and therapeutic tool for PD. Studies also need to describe the specific yoga practices used and any adverse effects of the practice to improve replicability and safety.


 » Conclusions Top


Based on the literature detailing the effect of Yoga on the autonomic nervous system, HPA axis, BDNF levels, and dopamine, we propose that Yoga has disease-modifying effects. Nevertheless, the physiological effects on the autonomic nervous system require regular, sustained, and long-term Yoga practice. Focus on the mindfulness aspect is what makes Yoga advantageous compared to mere physical activity. Adopting regular practice of Yoga by the population may help to reduce the risk of PD, especially in people at risk for PD. As a therapeutic tool, Yoga helps in improvement of gait, balance freezing, and falls. Yoga may also benefit depression, anxiety and memory disturbances in PD. More studies with larger sample sizes and longer follow-ups will be required to get clarity on the effect of Yoga. The impact of Yoga on sleep, cognition, autonomic features, and anxiety in PD needs further exploration. With the available evidence, Yoga shows promise as an add on therapy in PD, with standard yoga protocols and adherence as the key moderating factors.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

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