Effects of yoga-based interventions on cognitive function in healthy older adults: a systematic review of randomized controlled trials

Objective


Introduction
Aging is accompanied by a gradual decrease in mental capacity affecting cognitive ability.5][6][7] Despite the known benefits, physical activity levels decrease with age, 8 and this reduction in associated with worse physical and mental health. 9Adherence, commonly defined as participant completion of a prescribed exercise routine, is inconsistently reported in exercise studies examining older adults'. 10xploring new strategies and modes of physical activity that promote healthy aging and increase exercise adherence in older adults are important aspects of public health promotion.2][13] Different types of yoga emphasize these elements to a greater or lesser extent. 12In earlier research, older adults have described yoga as an enjoyable all-round workout suitable for their age group. 14Additionally, older adults report that participation in yoga has benefited their physical, mental, and social health. 159][20] There is some evidence that the health benefits of yoga-based interventions are comparable with those of aerobic exercise. 213][24] Recent reviews and meta-analyses show that yoga can benefit several mental and physical health outcomes in older populations, compared to both active and inactive control groups. 13,25,26However, reviews of yoga-based interventions on cognition are sparsely published and findings have been inconsistent.Two recent systematic reviews 27,28 and a meta-analysis 29 concluded that yoga interventions improved cognitive functions such as attention and processing speed, memory, and higher-order executive functions in a variety of populations, including older adults.However, another systematic review and meta-analysis 26 found no effect of yoga-based interventions on cognition in older adults.Chen et al., 30 showed that the effect of exercise on executive function in older adults was moderated by the type of exercise, and that yoga and tai chi interventions showed the second largest effect size (g = 0.38), after other forms of exercise (e.g.dance, coordination exercises) (g = 0.44), compared to resistance exercise (g = 0.22), aerobic exercise (g = 0.14), and combined exercise (g = 0.10).Another meta-analysis 2 found no association between yoga practice and cognition among older adults.
Within the context of public health and exercise prescription guidelines, it is important to understand yoga-based interventions characteristics from a physical activity perspective.Several authors 2,3,5,30 highlight the importance of exercise prescription variables being assessed in physical activity interventions to improve cognition.These variables, which include duration, frequency, intensity, and type of exercise, are referred to collectively as the FITT-principle. 31Here, we refer to them as 'intervention characteristics'.Cross-sectional and longitudinal data suggests that there is a relationship between exercise intensity and cognitive outcomes, 32 or lack of cognitive decline in older adults, with moderate and high intensity physical activity associated with less cognitive decline. 6Other parameters such as the mode, quality, and other dose-response variables may also moderate the effect of exercise on cognition, [33][34][35] but studies rarely report these variables. 26, [36][37][38] These omissions make it difficult to assess the effects of intervention characteristics on cognition.
Yoga-based interventions can be highly variable and often consist of several components beyond physical activity, such as breathing exercises and meditation practices, making these study characteristics important to document.It is necessary to understand the impact of the physical activity component in yoga-based interventions, as well as the impact of the other components, particularly as meditation practices alone have been found to have a positive effect on cognition in older adults. 39, 40 To our knowledge, no previous review has synthesized the findings from randomized controlled trials of the effects of yoga-based interventions on cognition in healthy older adults, including the characteristics of the yoga-based interventions.The main aim of this systematic review was to examine the effect of yoga-based interventions on cognitive functioning in adults aged ≥60.A secondary aim was to describe intervention characteristics and, where possible, the extent to which these influenced study outcomes.

Methods
We conducted a systematic review of the literature in accordance with Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, 41 which was pre-registered on Prospero July 25, 2019 (ID: CRD42020140158).
We enlisted the Karolinska University library to develop a detailed search strategy where multiple search terms were used for cognition (e. g. 'cognition', 'executive functioning', 'memory', 'attention', 'processing speed') with 'yoga', and 'elderly', 'older'.As Hatha yoga is an important component of the commonly studied Mindfulness-Based Stress Reduction (MBSR), Body Therapy (MBT) program, we also searched MBTSR AND cognition.Complete search terms are presented as Supplementary material 1.Additionally, individual searches in the abovementioned databases were performed; reference lists of retrieved articles were searched through by one reviewer (SH).

Eligibility criteria
The eligibility criteria for studies were as follows: (i) Participants: Healthy adults aged ≥60, free of known diseases and medical conditions; (ii) Intervention and comparison: Studies comparing yoga to active or no intervention control groups were included.Studies with a second yoga-based intervention as a control group, or studies involving mindfulness, meditation or breathing practices without including yoga postures were excluded; (iii) Outcomes: Studies that assessed one or more domains of cognitive functioning using a validated instrument.All validated neuropsychological tests were accepted as measures of cognitive function; (iv) Study design: Published and peer-reviewed experimental studies with a randomized controlled design that were written in English were included.Observational studies and other designs were excluded.Finally, there were no date restrictions.

Study selection
All records were screened by two independent reviewers (J Ö, SH) and were carried out in two stages.First, title and abstract were screened using Endnote reference managing software (version X9, Clarivate Analytics, 2018) where duplicates and obviously irrelevant studies were removed.Second, full texts of studies passing the first stage were screened in further detail.A third reviewer (MH) was called upon when a decision could not be made regarding an article's eligibility.Further details are shown in Fig. 1.

Analysis
Data was extracted and compiled into a table presenting study characteristics (Table 1).For quantitative outcomes available across three or more trials, a meta-analysis was planned to estimate the pooled effects of the yoga-based interventions compared to controls.However, due to heterogeneity of the studies, data were instead synthesized using a formal narrative approach.

Risk of bias assessment
Risk of bias was assessed independently by two researchers (J Ö, SH) using the revised Cochrane risk of bias (RoB) tool, version 2. 43 The assessed domains were: randomization process (selection bias), deviations from intended interventions (performance bias), missing outcome data (attrition bias), measurement of the outcome (measurement bias), selection of the reported result (reporting bias), and overall bias.Under each domain, studies were classified as 'low', 'some concerns' or 'high' risk of bias.The final judgement of each reviewer followed the algorithm guide as part of the revised RoB 2 tool.Discrepancies were resolved through a third reviewer (MH), who was blinded to the other researchers' assessments.

Results
A total of 1466 records were initially identified through the data searches.After the first stage of screening, 22 articles were retrieved for full-text review.Out of these, only five studies were included in the systematic review.The second search gave 399 records, of which 10 were retrieved for full-text review.None of these articles were included, nor from the searches through reference lists.One of the additional searches resulted in the inclusion of one article.In total, six articles including five original studies were identified for final inclusion; see Fig. 1.

Study and participant characteristics
The six articles included were RCTs from the USA, [44][45][46] India, 47,48 Lithuania, 49 and multiple countries from the Asia Pacific region and Africa. 48The number of participants ranged from 33 to 792; mean age = 62-76 years.Most participants were female ranging between 60-90 % of the study populations.Only one study 48 had an even distribution between men and women.All study details are shown in Table 1.

Intervention characteristics
The yoga intervention characteristics (type, frequency, duration, intensity, length of intervention) varied between studies with; 1-7 sessions per week, 40− 90 min per session, and the length of intervention varying between 8-260 weeks.Three studies used hatha yoga, 44,45,47,48 one study used iyengar yoga, 46 and one did not specify the style of yoga. 49The intensity level was not reported in any of the included studies.All studies stated that the yoga-based interventions included meditation practices and breath awareness techniques, however, the proportion of each component (physical postures, breathing, and meditation exercises) was not specified.All interventions were delivered in person by a qualified yoga instructor.Home practice was included in two of the studies, but was not the primary mode of delivery 46,47 (Table 1).A variety of cognitive test batteries and assessments were reported.All trials assessed cognition at pre-intervention and post-intervention.
Adherence to the yoga-based interventions were reported by instructors in three studies, [44][45][46] and through self-reports in one study. 46hree studies [47][48][49] did not specify the method of reporting.Three of the studies (two unique trials) included an active control group comprising exercise [44][45][46] ; one was a stretching-strengthening group who showed similar adherence rates to the yoga group, 44,45 and the other an aerobic exercise group showing lower adherence rates than the yoga group. 46owever, difference between the yoga and the exercise group did not reach statistical significance. 50dverse events were reported in three [44][45][46][47] out of the six included studies.One study 46 reported a single adverse event in both the yoga and aerobic exercise groups, respectively.Adverse events were mild muscle-skeletal injuries.Three studies reported no adverse events. 44,45,47

Effects on cognition
Four studies reported significant effects of the yoga-based intervention on cognition from pre-to post-intervention 44,45,47,48 and two did not. 46,49Changes favoring the yoga-based intervention compared to control were found for working memory capacity, 44,47 visual and verbal memory 47 and efficiency of mental set shifting and flexibility, 44 improved attentional 45 and information processing abilities. 45,47dditionally, significant improvements following a yoga-based intervention were found in gross memory functioning and visual, verbal, recall, recognition, immediate and delayed everyday memory. 48n an 8-week trial involving 118 healthy community-dwelling older adults, Gothe et al. 44 assessed executive functions by comparing a yoga-based intervention to stretch-strengthening exercises.Compared to the stretch-strengthening group, there was a significant pre-post improvement in working memory capacity, and efficiency of mental set shifting and flexibility, following the yoga-based intervention, with effect sizes ranging from small to moderate. 51Another article 45 from the same 8-week trial reported significant improvements following the yoga-based intervention in attentional and information processing abilities, with medium to large effect sizes. 52Hariprasad et al., 47 conducted a six-month trial involving 87 aged-care residents and reported significant pre-post improvements in working memory capacity, visual and verbal memory and information processing.following the yoga-based intervention compared to a no-intervention control group.In a five year trial involving 792 older adults, Pandya 48 reported significant improvements following a yoga-based intervention in gross memory functioning and visual, verbal, recall, recognition, immediate, and delayed everyday memory (medium effect sizes).Additionally, regular attendance and self-practice were reported as strong moderators of the efficacy of the yoga-based intervention on cognitive function.
Oken et al. 46 conducted a six-month trial (n = 118) comparing a yoga-based intervention to both walking exercise and a waitlist control group.No significant effects of the yoga-based intervention were found on cognitive functions or alertness measures.Similarly, Čekanauskaitè et al. 49 also reported no significant effect following a 10-week yoga-based intervention on cognition in 33 older adults.

Risk of bias results
A summary of the risk of bias assessment of each study is presented in Fig. 2. Each study was assessed based on the obtained journal article, and the reviewers assessed the effect of assignment to intervention.Three of the assessed domains (deviations from intended interventions, measurement of the outcome, and selection of the reported result) were judged with 'some concern' or 'high' risk of bias in the majority of the included articles, which resulted in an overall 'high' risk of bias for all studies.This was mainly due to the lack of prospectively registered protocols and the absence of information regarding the signaling questions for each domain.None of the included studies were able to blind the participants or yoga instructors from the intervention, therefore this parameter was not included in our risk of bias assessment.Further detailed information is provided as Supplementary material 2.

Summary of evidence
The main aim of this systematic review was to summarize evidence from RCTs reporting the effects of a yoga-based intervention on cognitive functioning in healthy older adults.Four 44,45,47,48 of the six reviewed articles reported significant improvements following engagement with a yoga-based intervention in several aspects of cognitive functioning including: attention, processing speed, memory, and executive function.Effect sizes were reported in three 44,45,48 of the four articles (range = small to large).In the two studies where a yoga-based interventions were not found to impact cognitive functioning in healthy older adults, the authors 46 hypothesized that this occurred because all the participants were healthy and had good cognitive function at baseline (ceiling effect).However, in the three articles where yoga was found to influence cognition, 44,45,48 participants also did not report any cognitive impairments at baseline.This current review excluded studies with participants recruited on the basis of a specific disease or medical condition.However, in the Hariprasad et al., 47 study, where yoga was found to influence cognition, most of the participants reported subjective memory complaints at baseline.This occurred despite the researchers initial screening and exclusion of individuals with symptoms of dementia, depression, and psychiatric disorders.This is consistent with findings in a recent scoping review by Gretchen and colleagues 53 which showed improved cognitive function among older adults with mild cognitive impairment following a yoga-based intervention.The other three articles, 44,45,48 where yoga was found to influence cognition, did not report any cognitive impairment among participants at baseline.Future studies could address this issue by using appropriate screening methods and by stricter inclusion and exclusion criteria, as well as specifying population characteristics in the results.Another recent systematic review 28 that examined yoga-based intervention effect on cognition and mental health in elderly populations drew a similar conclusion, naming the use of valid screening tools as a key component for future research.
The yoga-based intervention used by Čekanauskaitès et al. 49 did not impact self-reported stress levels measured by the Perceived Stress Scale.Indeed, previous work 54 shown that objectively measured stress (cortisol), and self-reported stress and anxiety symptoms, mediate the impact of yoga on cognition.6][57][58][59] .In their meta-analysis, Gothe & McAuley 29 argue for future research to examine the effect of yoga on the stress response in relation to cognitive functioning, which is a limitation in the current work and an important area for future research.
A secondary aim of this review was to examine the characteristics of yoga-based interventions, and to describe any associations between these criteria and cognitive outcomes.Shorter duration interventions reported higher adherence compared to longer interventions, however there were no significant differences in adherence rates between yoga groups and the exercise-based control groups, indicating that yoga is equally acceptable to older adults as other forms of exercise.Only one study reported that adherence and self-practice moderated the effect on cognitive function. 48We advocate that future studies should report adherence to the yoga programs, specifying the definition applied. 10pecifically, objective assessments of intervention adherence should be used where possible, and the impact of supervised compared to non-supervised programs on adherence should be further explored.
The yoga-based intervention varied with regard to the style of practice delivered, frequency and duration of classes, and the length of intervention.The proportion of each component (physical postures, breathing, and meditation exercises) were not specified in any studies.This is important to address because some breathing and meditation exercises are unique to yoga and may impact study findings.Intensity levels were not reported in any of the included studies.Given that the intensity of physical activity has been shown to be important in determining cognitive improvements following other exercise interventions, 32 we propose that the intensity of yoga-based physical activity should be considered in the design and reporting of future studies.Indeed, different styles of yoga differ in their intensity level 38 and the relationship between heart rate and oxygen consumption in yoga-based exercise is non-linear (compared to the linear relationship in aerobic exercise), which suggests there is a need to create a standard for reporting intensity levels from yoga interventions. 38We support this recommendation and previous work which highlights an overall need for better reporting of intervention characteristics. 60,61We suggest that reporting should follow the TIDieR template for intervention description and replication. 62As Etnier and colleagues 35 point out; "a better understanding of underlying mechanisms and accurate reporting and coding of variables will serve future research within this field".

Strengths and limitations
This is the first systematic review to study the impact of yoga-based interventions on cognitive function in healthy older adults.Strengths of the study include: i) the assessment of intervention characteristics using the FITT criteria; ii) the review was conducted in concordance with an established systematic review framework and reported using PRISMA guidelines; and iii) the inclusion of only RCTs helped ensure that the reviewed studies are consistent with best practice recommendations.Some potential limitations are also acknowledged.As only six studies were included and these were heterogeneous, both in terms of study design and outcomes, our ability to draw definitive conclusions regarding effects of yoga-based interventions on cognitive functioning in this population is limited.The majority of studies had relatively low numbers of participants.Three [44][45][46] studies included an active comparison group, while three [47][48][49] included a waitlist or a no-intervention control group.Therefore, in half the studies reviewed, it is unclear whether the effects are attributable to the yoga-based intervention or to non-specific factors, such as time/attention effects.Furthermore, we only included studies published in English, and therefore might have overlooked research published in other languages.Finally, none of the reviewed studies assessed cognitive function at multiple follow-up time points; therefore the long term impact of yoga-based interventions on cognition are unknown. 29

Conclusions
Yoga-based interventions show potential to improve cognition in healthy older adults.However, there are currently few published studies on the topic, all with a high risk of bias.Adequately powered RCTs with robust study designs and long-term follow-ups are required using validated screening tools and cognitive assessments.Future studies should explicitly report the intervention characteristics, and where possible, demonstrate how these moderate study outcomes.Yoga-based exercise includes physical components that are important for healthy ageing, such as balance and flexibility.Given the ageing of populations worldwide, the application of yoga to help prevent and treat cognitive decline warrants further investigation.

Funding
This review was supported by a grant from the Swedish Research Council for Health, Working Life and Welfare (FORTE), grant number 2017-00024, awarded to MH.The funding source had no influence on the design or conduct of the review.

Table 1
Participant and study characteristics.