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7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 113
A systematic review of randomised control trials on the effects of yoga
on stress measures and mood
Michaela C Pascoe a Isabelle E Bauer b
a Institute of Neuroscience and Physiology Dept of Clinical Neuroscience and Rehabilitation Sahlgrenska Academy at University of Gothenburg Swedenb University of Texas Health Science Center Department of Psychiatry and Behavioral Science Houston TX USA
a r t i c l e i n f o
Article history
Received 12 February 2015
Received in revised form
10 July 2015
Accepted 10 July 2015
Keywords
Yoga
Anxiety
Depression
Mood
Stress
Brain imaging
In1047298ammation
Exercise
a b s t r a c t
Stress related disorders such as depression and anxiety are leading sources of disability worldwide and
current treatment methods such as conventional antidepressant medications are not bene1047297cial for all
individuals There is evidence that yoga has mood-enhancing properties possibly related to its inhibitory
effects on physiological stress and in1047298ammation which are frequently associated with affective disor-
ders However the biological mechanisms via which yoga exerts its therapeutic mood-modulating effects
are largely unknown This systematic review investigates the effects of yoga on sympathetic nervous
system and hypothalamic pituitary adrenal axis regulation measures It focuses on studies collecting
physiological parameters such as blood pressure heart rate cortisol peripheral cytokine expression and
or structural and functional brain measures in regions involved in stress and mood regulation Overall
the 25 randomised control studies discussed provide preliminary evidence to suggest that yoga practice
leads to better regulation of the sympathetic nervous system and hypothalamic-pituitary-adrenal sys-
tem as well as a decrease in depressive and anxious symptoms in a range of populations Further
research is warranted to con1047297rm these preliminary 1047297ndings and facilitate implementation in clinical
settings
copy 2015 Elsevier Ltd All rights reserved
1 Introduction
11 Mood stress and brain changes
Unipolar depression and anxiety are the leading source of adult
disability worldwide (Shyn and Hamilton 2010 Whiteford et al
2013) Approximately 350 million people are estimated to suffer
from depression (World Health Organisation [WHO] 2013) and
associated societal costs are V92 billion in Europe alone (Wittchen
et al 2011 Gustavsson et al 2011 Olesen et al 2012) Depressionand anxiety are highly co-morbid with each other and have shared
aetiology and neurobiology (Neale and Kendler 1995) Anxiety is the
single strongest predictor of depression onset (Mathew et al 2011
Avenevoli et al 2001 Hranov 2007) While there are neurochem-
ical differences between the conditions recent studies view
depression and anxiety as overlapping syndromes existing on a
continuum (Hranov 2007 Baldwin et al 2002 Ionescu et al 2013)
Depression and anxiety are closely linked to structural and
functional abnormalities in a number of stress and mood related
brain regions (Drevets 1998 Davidson 2003 Siegle et al 2002
Abercrombie et al 1998 Drevets 1999 Eren et al 2003) Alter-
ations have been observed in the anterior cingulate cortex (ACC)
(involved in immune response (Capuron et al 2005 Craig 2003
Goehler et al 2000 Gaykema and Goehler 2011) affective regu-
lation and reward anticipation ( Jackson et al 2006 Decety and Jackson 2004)) and the prefrontal cortex (PFC) (which anatomi-
cally connects to the ACC and is involved in social behaviour and
personality traits (Miller et al 2002 Yang and Raine 2009))
Functional and structural changes are also seen in regions of the
limbic system (involved in the stress response regulations of fear
anxiety mood and emotion (Herman et al 2005 Kempton et al
2011 Davis 1992)) namely the hippocampus and amygdala
Men with a 1047297rst-episode major depression show smaller hip-
pocampal total and gray matter volumes than healthy men ( Frodl
et al 2002) In monozygotic twins a smaller hippocampal volume
has been found to be a risk factor for the development of
Corresponding author Institute of Neuroscience and Physiology Dept of Clin-
ical Neuroscience and Rehabilitation Sahlgrenska Academy at University of Goth-
enburg Box 440 SE-405 30 Gothenburg Sweden
E-mail address michaelapascoeneuroguse (MC Pascoe)
Contents lists available at ScienceDirect
Journal of Psychiatric Research
j o u r n a l h o m e p a g e w w w e l s e v i e r c om l o c a t e p s y c h i r e s
httpdxdoiorg101016jjpsychires201507013
0022-3956copy
2015 Elsevier Ltd All rights reserved
Journal of Psychiatric Research 68 (2015) 270e282
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posttraumatic stress disorder Additionally recent models of neu-
roprogression suggest that the hippocampal atrophy observed in
unipolar depression is cumulative as the degree of atrophy appears
to be related to the number of untreated episodes and illness
duration (Sheline et al 2003 Berk et al 2011 Fries et al 2012)
One could therefore argue that the relationship between structural
brain abnormalities and affective disorders is bidirectional
The aetiology of depressive and anxious disorders are complex
and polygenetic and additional to structural abnormalities in-
dividuals show abnormalities in the function and expression of
monoamine neurotransmitters such as serotonin and dopamine
(Krishnan and Nestler 2008 Morilak and Frazer 2004) increased
oxidative stress (Michel et al 2012 Bouayed et al 2009) decreased
expression of the neurotropic protein brain-derived neurotrophic
factor (BDNF) (Autry and Monteggia 2012) and changes in the
expression of cytokines (Dantzer 2012) Cytokines are small cell
signalling protein molecules essential in the innate immune
response and in1047298ammation Cytokines can be either pro or anti-
in1047298ammatory (del Zoppo et al 2000) and among other functions
stimulate the autonomic nervous system (ANS) and the hypotha-
lamic pituitary adrenal (HPA) axis (Silverman and Sternberg 2012)
The ANS has two main divisions the parasympathetic nervous
system (PNS) and the sympathetic nervous system (SNS) TheSNS isinvolved in the mobilisation of the body in situations of stress to
either lsquo1047297ght or 1047298ightrsquo the stressor The PNS is responsible for
returning the body to a homoeostatic state after the activation of
the SNS (Buijs 2013) In many cases the PNS and SNS have com-
plementary and opposing actions in that one system is responsible
for activating a physiological response and the other is responsible
for inhibiting it (Buijs 2013) Activation of the SNS is associated
with a number of physiological changes including increased heart
rate blood pressure HPA axis activation and subsequent down-
stream release of the glucocorticoid hormone cortisol from the
adrenal cortex (Raison et al 2006) Glucocorticoid levels and the
further synthesis of pro-in1047298ammatory cytokines are normally
regulated by a HPA axis negative feedback mechanism (Silverman
and Sternberg 2012)The reciprocal relationship among stress HPA axis regulation
and depression and anxiety is well known (Dantzer 2012 Dantzer
et al 2008 Maes 2008a) Clinical depression and anxiety are
associated with an increased in1047298ammatory state These conditions
are characterized by dysfunctional glucocorticoid feedback inhibi-
tion (Silverman and Sternberg 2012) hypersecretion of CRH HPA
axis dysfunction (Boyer 2000 Roy-Byrne et al 1986) increased
circulatory cortisol (a widely used biomarker of HPA axis dysfunc-
tion) (Olson et al 2012) and production of pro-in1047298ammatory cy-
tokines (Silverman and Sternberg 2012 Raison et al 2006
Sapolsky et al 2000 King and Hegadoren 2002) Anxiety related
sustained central arousal has been proposed to deplete neuro-
transmission in the forebrain and thus precipitate the onset of
depression (Neale and Kendler 1995 Eison 1990 Johnson et al1990 Nutt et al 1998 Schulberg et al 1998)
On the other hand chronic stress and in1047298ammation can
contribute to the onset of depressive and anxious symptoms
(Dantzer 2012 Masi and Brovedani 2011 Pascoe et al 2011)
Treatment with the in1047298ammatory cytokine Interferon-a (INF-a)
(Capuron and Miller 2004) has been associated with the presen-
tation of depressive and anxious symptoms in cancer survivorships
(Capuron et al 2002) These depressive symptoms resolve with
INF-a therapy termination (Capuron and Dantzer 2003) and anti-
depressant medication (Musselman et al 2001)
Finally the bene1047297cial effects of pharmaceutical antidepressant
medications appear to relate to their in1047298uence on in1047298ammatory
activity Tricyclic antidepressant medications reduce pro-
in1047298
ammatory Interleukin-1 (IL-1) and Interleukin-2 (IL-2) and
increase anti-in1047298ammatory Interleukin-10 in animal models
(Kubera et al 2000) suggesting that these pharmaceutical anti-
depressant medications likely reduce depressive symptoms at
least in part by mediating mood modulating in1047298ammatory
markers (Kubera et al 2000) Additionally high basal in1047298amma-
tion is associated with a treatment resistance to pharmaceutical
anti-depressant interventions in clinical populations An
increased in1047298ammatory state as characterised by heightened
plasma concentrations of in1047298ammatory cytokines and acute phase
proteins prior to antidepressant treatment is associated with a
non-response (Maes 2008b Raison et al 2013)
Not only are current pharmacological treatment methods such
as selective serotonin reuptake inhibitors (SSRI) not bene1047297cial for
all individuals (Howland 2006 Kirsch et al 2008) these medica-
tions are associated with deleterious side effects such as metabolic
disorders and diabetes (McIntyre et al 2010) that reduce quality of
life and negatively in1047298uence individual adherence to the medica-
tion (Schatzberg 2007) Thus there is need for safer and more
effective treatment methods for mood disorders
12 Yoga is an effective treatment for depressive and anxious
symptomatology
The termyogais Sanskrit for lsquounionrsquo or lsquoto yokersquo and describes a
lifestyle aiming to achieve union of mind body and spirit While the
origins of yoga are unclear the Indian sage Patanjali described eight
limbs of yoga (G F 1998) which have been performed in Eastern
cultures for thousands of years In recent years yoga has become
increasingly popular in Western cultures (Ding and Stamatakis
2014 Tindle et al 2005) There are many forms of yoga each
with unique approaches and theoretical underpinnings making a
de1047297nitive taxonomy dif 1047297cult (Ospina et al 2007) Previous authors
have noted that this lack of a de1047297nitive de1047297nition and subsequent
differences in the forms studied has hampered neuroscienti1047297c
research in this 1047297eld (Lutz et al 2007) All forms of yoga however
share common elements including use of controlled breathing
(pranayama) physical postures (asanas) and meditative techniques(dhyana) to achieve well-being and mind body union and balance
(Farmer 2012 P1047298ueger 2011 Travis and Pearson 2000) Several
studies and systematic reviews demonstrate the mood enhancing
effects of yoga as treatments for clinical depression ( Uebelacker
et al 2010 Pilkington et al 2005 DSilva et al 2012
Balasubramaniam et al 2012) and anxiety (Chattha et al 2008
Granath et al 2006 Banerjee et al 2007 Harinath et al 2004
Kjellgren et al 2007 West et al 2004 Woolery et al 2004
Smith et al 2007 Li and Goldsmith 2012) Yoga practice is asso-
ciated with a reduced number of major depressive episodes and
lower risk for dysthymia which is a milder but longer-term form of
depression (Banerjee et al 2007 Kjellgren et al 2007 Woolery
et al 2004 John et al 2007 Sharma et al 2006 Butler et al
2008) Meta-analyses and systemic reviews indicate that yogaand meditative therapies are equally effective as conventional an-
tidepressants in the treatment of depressive and anxious disorders
(da Silva et al 2009 Cramer et al 2013 Chen et al 2012) The
limited data thus far suggests that these practices are associated
with changes in the stress response (Kinser et al 2012 McCall
2013) The neurobiological mechanisms however via which yoga
exerts its mood enhancing effects are still not clearly understood
2 Methods
21 Systematic search strategy
In the present study we aimed to systematically review rand-
omised control trials (RCTs) investigating the effects of yoga on
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 271
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stress-related biological measures and their neural correlates in
the context of depressive and anxious symptomology We searched
Pubmed MedlineOvid and Scopus with no year restriction for ar-
ticles containing the speci1047297c title word lsquoyogarsquo and the speci1047297c
abstract word lsquodepression rsquo lsquomoodrsquo lsquoanxietyrsquo lsquodepressive rsquo lsquoaffectiversquo
or lsquoanxiousrsquo and lsquoimmunersquo lsquocortisolrsquo lsquocatecholaminesrsquo lsquonorepi-
nephrinersquo lsquocytokinersquo lsquointerleukinrsquo lsquoInterferonrsquo lsquotumour necrosis
factor-alpharsquo lsquobrain-derived neurotropic factorrsquo lsquodopaminersquo lsquosero-
toninrsquo lsquoblood pressurersquo or lsquoheart ratersquo To explore the neural cor-
relates of stress in relation with yoga we searched the speci1047297c
abstract word lsquobrainrsquo and with the speci1047297c abstract words lsquomag-
netic resonance imaging (MRI)rsquo lsquofunctional MRIrsquo lsquodiffusion tensor
imaging (DTI)rsquo lsquoEEGrsquo lsquospectroscopyrsquo lsquoresting state fMRIrsquo lsquomagnetic
resonance spectroscopy (MRS)rsquo lsquopositron emission tomography
(PET)rsquo or lsquoarterial spin labelling (ASL)rsquo Articles reviewed were
restricted to original RCTs published in English that included a
population who engaged in a yoga practice with outcome mea-
sures related to HPA axis activation in1047298ammation or brain imaging
in conjunction with a measure of mood or current affective state
Review papers non-randomised trials case series and disserta-
tions were excluded
3 Results
A total of 122 papers with stress-related physiological parame-
ters were initially retrieved Studies were screened using title and
abstract when required full texts were accessed (n frac14 76) Nine of
these were excluded as they were review articles A further 31
papers were excluded as they were quasi-experimental cross
sectional of cohort studies four were excluded as they did not
include a biological and mood related outcome and 1047297ve were
excluded as they did not involve a yoga based intervention Three
additional papers were excluded as their results have not yet been
published Thus 24 RCT trials were included in the1047297nal review The
details of the search strategy are depicted in Fig 1
A total of 50 brain imaging papers were initially retrieved 34
were duplicates and were removed a further four were reviews
leaving 12 articles that were screened for eligibility seven were
removed as they did not include a brain imaging outcome one was
removed as it did not include a yoga asana intervention Three
further articles were removed as they were not RCTs Thus one RCT
trial was included in the 1047297nal review The details of the search
strategy are depicted in Fig 2
31 Characteristics of the included trials
Reviewed study characteristics are outlined in Table 1 Twenty-
1047297ve RCTs examining the effects of yoga on biological outcomes in
conjunction with mood related or brain related measures have
been included in this review Eight RCTs originated from India
(Sujatha and J A 2014 McDermott et al 2014 Kanojia et al 2013Ebnezar et al 2012 Gopal et al 2011 Telles et al 2010 Vadiraja
et al 2009 Malathi et al 1998) nine from the United States
(Woolery et al 2004 Corey et al 2014 Chandwani et al 2014
Kiecolt-Glaser et al 2014 Field et al 2013 Innes and Selfe
2012 Banasik et al 2011 Streeter et al 2010a) two from Australia
(Smith et al 2007 Cheema et al 2013) two from the United
Kingdom (Newham et al 2014 Bowden et al 2012) one from
Fig 1 Flow chart showing the retrieval process of biological related trials included in the systematic review
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282272
7262019 documento cientifico de la Yogapdf
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Germany (Sarubin et al 2014)onefrom Spain (Tolbanos Roche and
Mas Hesse 2014) one from Sweden (Hallgren et al 2014) and two
from Brazil (Danucalov et al 2013 Rocha et al 2012)
The studied populations were heterogeneous across trials three
involved individuals with depression (Woolery et al 2004 Fieldet al 2013 Sarubin et al 2014) one focused on healthy in-
dividuals experiencing mildmoderate stress (Smith et al 2007)
one studied individuals with alcohol dependence (Hallgren et al
2014) and one involved 1047298ood survivors (Telles et al 2010) Four
studied people with illnesses commonly comorbid to mood disor-
ders such as metabolic problems (McDermott et al 2014 Corey
et al 2014) and hypertension (Sujatha and J A 2014 Tolbanos
Roche and Mas Hesse 2014) Six trials focused on individuals
with medical conditions such as restless leg syndrome (Innes and
Selfe 2012) cancer survivorships (Vadiraja et al 2009
Chandwani et al 2014 Kiecolt-Glaser et al 2014 Banasik et al
2011) and osteoarthritis (Ebnezar et al 2012) One study involved
healthy military personal (Rocha et al 2012) Finally eight studies
involved healthy adults (Kanojia et al 2013 Gopal et al 2011Malathi et al 1998 Streeter et al 2010a Cheema et al 2013
Newham et al 2014 Bowden et al 2012) including familial
caregivers (Danucalov et al 2013)
Hatha yoga was the most common intervention and was used in
six trials (Smith et al 2007 Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Cheema et al 2013 Sarubin et al 2014 Danucalov
et al 2013) Iyengar yoga was the second most common inter-
vention and was used in 1047297ve trials (Woolery et al 2004 Innes and
Selfe 2012 Banasik et al 2011 Streeter et al 2010a Bowden et al
2012) while two trials used prenatal yoga (Field et al 2013
Newham et al 2014) One trial used restorative yoga (Corey et al
2014) one used Patanjali yoga (Telles et al 2010) four did not
specify the yoga form yet provided the sequence in the method-
ology (McDermott et al 2014 Kanojia et al 2013 Ebnezar et al
2012 Chandwani et al 2014) and six did not specify the yoga
form or clearly outline the sequence used (Gopal et al 2011
Vadiraja et al 2009 Malathi et al 1998 Tolbanos Roche and
Mas Hesse 2014 Hallgren et al 2014 Rocha et al 2012)
The most common stress-related biological measures (n frac14 11studies) were autonomic arousal measures including blood pres-
sure heartrate skinconductanceand respiration (Smithet al 2007
Sujatha and J A 2014 McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Gopal et al 2011 Telles et al 2010 Innes
and Selfe 2012 Tolbanos Roche and Mas Hesse 2014 Yeung et al
2014 Cheema et al 2013) Heart rate variability (HRV) was
measured in two studies as an indicator of ANS function and car-
diovascular response (Telles et al 2010 Cheema et al 2013)
increased HRV is interpreted to indicate greater parasympathetic
nervous system activity and a healthy balance between the sym-
pathetic and parasympathetic nervous systems (Buijs 2013)
The steroid hormone cortisol was assessed in 13 trials (Woolery
et al 2004 Gopal et al 2011 Vadiraja et al 2009 Corey et al
2014 Chandwani et al 2014 Field et al 2013 Banasik et al2011 Newham et al 2014 Bowden et al 2012 Sarubin et al
2014 Hallgren et al 2014 Danucalov et al 2013 Rocha et al
2012) Cytokines were measured in two trials (Gopal et al 2011
Kiecolt-Glaser et al 2014) Some other relevant health related
measures included lipid pro1047297les and body mass index (Sujatha and
J A 2014 McDermott et al 2014) As outlined in Table 1 all trials
included some measure of depressive symptoms except Sujatha
et al Smith et al Malathi et al and Ebnezar et al (Smith et al
2007 Sujatha and J A 2014 Ebnezar et al 2012 Malathi et al
1998) and 16 studies included a measure of anxiety (Woolery
et al 2004 Smith et al 2007 Sujatha and J A 2014 Ebnezar
et al 2012 Gopal et al 2011 Telles et al 2010 Vadiraja et al
2009 Field et al 2013 Innes and Selfe 2012 Streeter et al
2010a Cheema et al 2013 Newham et al 2014 Tolbanos Roche
Fig 2 Flow chart showing the retrieval process of imaging related trials included in the systematic review
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 273
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7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 613
7262019 documento cientifico de la Yogapdf
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and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 277
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 279
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more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Nutt D Argyropoulos S F S 1998 Generalized Anxiety Disorder DiagnosisTreatment and its Relationship to Other Anxiety Disorders Martin Dunitz Ltd London
Olesen J et al 2012 The economic cost of brain disorders in Europe Eur J Neurol19 (1) 155e162
Olson KL Marc DT Grude LA McManus CJ Kellermann GH 2012 Thehypothalamic-pituitary-adrenal axis the actions of the Central Nervous Systemand Potential Biomarkers In Klatz R Goldman R (Eds) Anti-aging Thera-peutics vol XIII American Academy of Anti-Aging Medicine Chicago IL USApp 91e100 201
Organisation WH 2013 Depression FactsheetOspina MB et al 2007 Meditation practices for health state of the research Evid
Rep Technol Assess (Full Rep) (155) 1e263Pascoe MC et al 2011 In1047298ammation and depression why poststroke depression
may be the norm and not the exception Int J Stroke 6 (2) 128e135Penman S et al 2012 Yoga in Australia results of a national survey Int J Yoga 5
(2) 92e101P1047298ueger LW 2011 Yoga body the origins of modern posture practice Relig Stud
Rev 37 (3) 235e235Piet J Hougaard E 2011 The effect of mindfulness-based cognitive therapy for
prevention of relapse in recurrent major depressive disorder a systematic re-
view and meta-analysis Clin Psychol Rev 31 (6) 1032e
1040Pilkington K et al 2005 Yoga for depression the research evidence J AffectDisord 89 (1e3) 13e24
Poll EM et al 2007 Saliva collection method affects predictability of serumcortisol Clin Chim Acta 382 (1e2) 15e19
Raison CL et al 2013 A randomized controlled trial of the tumor necrosis factorantagonist in1047298iximab for treatment-resistant depression the role of baselinein1047298ammatory biomarkers JAMA Psychiatry 70 (1) 31e41
Raison CL Capuron L Miller AH 2006 Cytokines sing the blues in1047298ammationand the pathogenesis of depression Trends Immunol 27 (1) 24e31
Rocha KK et al 2012 Improvement in physiological and psychological parame-ters after 6 months of yoga practice Conscious Cogn 21 (2) 843e850
Roy-Byrne PP et al 1986 The corticotropin-releasing hormone stimulation test inpatients with panic disorder Am J Psychiatry 143 (7) 896e899
Sapolsky RM Romero LM Munck AU 2000 How do glucocorticoids in1047298uencestress responses Integrating permissive suppressive stimulatory and pre-parative actions Endocr Rev 21 (1) 55e89
Sarubin N et al 2014 The in1047298uence of Hatha yoga as an add-on treatment inmajor depression on hypothalamic-pituitary-adrenal-axis activity a random-
ized trial J Psychiatr Res 53 76e
83Schatzberg AF 2007 Safety and tolerability of antidepressants weighing the
impact on treatment decisions J Clin Psychiatry 68 (Suppl 8) 26e34Schulberg HC Katon WJ S MK 1998 Management of mood and anxiety dis-
orders in primary care In Rush AJ (Ed) Mood and Anxiety Disorders CurrentScience Inc Philadelphia PA
Sharma VK et al 2006 Effect of Sahaj Yoga on neuro-cognitive functions in pa-tients suffering from major depression Indian J Physiol Pharmacol 50 (4)375e383
Sheline YI Gado MH Kraemer HC 2003 Untreated depression and hippo-campal volume loss Am J Psychiatry 160 (8) 1516e1518
Shyn SI Hamilton SP 2010 The genetics of major depression moving beyondthe monoamine hypothesis Psychiatr Clin North Am 33 (1) 125e140
Siegle GJ et al 2002 Cant shake that feeling assessment of sustained event-related fMRI amygdala activity in response to emotional information indepressed individuals Biol Psychiatry 51 (9) 693e707
da Silva TL Ravindran LN Ravindran AV 2009 Yoga in the treatment of moodand anxiety disorders a review Asian J Psychiatr 2 (1) 6e16
Silverman MN Sternberg EM 2012 Glucocorticoid regulation of in1047298ammationand its functional correlates from HPA axis to glucocorticoid receptordysfunction Ann N Y Acad Sci 1261 55e63
Smith C et al 2007 A randomised comparative trial of yoga and relaxation toreduce stress and anxiety Complement Ther Med 15 (2) 77e83
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern Complement Med16 (11) 1145e1152
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern ComplementaryMed 16 (11) 1145e1152
Streeter CC et al 2012 Effects of yoga on the autonomic nervous system gamma-aminobutyric-acid and allostasis in epilepsy depression and post-traumaticstress disorder Med Hypotheses 78 (5) 571e579
Sujatha T J A 2014 Efectivenes of a 12-Wek yoga program on physiopsychologicalparameters in patients with hypertension Int J Pharm Clin Res 6 (4)329e335
Telles S et al 2010 Post traumatic stress symptoms and heart rate variability inBihar 1047298ood survivors following yoga a randomized controlled study BMCPsychiatry 10 18
Tindle HA et al 2005 Trends in use of complementary and alternative medicineby us adults 1997-2002 Altern Ther Health Med 11 (1) 42e49
Tolbanos Roche L Mas Hesse B 2014 Application of an integrative yoga therapyprogramme in cases of essential arterial hypertension in public healthcareComplement Ther Clin Pract 20 (4) 285e290 httpdxdoiorg101016
jctcp201410004Travis F Pearson C 200 0 Pure consciousness distinct phenomenological and
physiological correlates of ldquoconsciousness itself rdquo Int J Neurosci 100 (1e4)77e89
Uebelacker LA et al 2010 Hatha yoga for depression critical review of the evi-dence for ef 1047297cacy plausible mechanisms of action and directions for futureresearch J Psychiatr Pract 16 (1) 22e33
Vadiraja HS et al 2009 Effects of a yoga program on cortisol rhythm and moodstates in early breast cancer patients undergoing adjuvant radiotherapy arandomized controlled trial Integr Cancer Ther 8 (1) 37e46
Wardle J Adams J Sibbritt D 2014 Referral to yoga therapists in rural primaryhealth care a survey of general practitioners in rural and regional New SouthWales Australia Int J Yoga 7 (1) 9e16
Weibel L 2003 Methodological guidelines for the use of salivary cortisol as bio-logical marker of stress Presse Med 32 (18) 845e851
West J et al 2004 Effects of Hatha yoga and African dance on perceived stressaffect and salivary cortisol Ann Behav Med 28 (2) 114e118
Whiteford HA et al 2013 Global burden of disease attributable to mental andsubstance use disorders 1047297ndings from the global Burden of Disease Study 2010Lancet 382 (9904) 1575e1586
Wittchen HU et al 2011 The size and burden of mental disorders and otherdisorders of the brain in Europe 2010 Eur Neuropsychopharmacol 21 (9)655e679
Woolery A et al 2004 A yoga intervention for young adults with elevatedsymptoms of depression Altern Ther Health Med 10 (2) 60e63
Yang Y Raine A 2009 Prefrontal structural and functional brain imaging 1047297ndingsin antisocial violent and psychopathic individuals a meta-analysis PsychiatryRes 174 (2) 81e88
Yeung A et al 2014 Randomised controlled trial of a 12 week yoga intervention
on negative affective states cardiovascular and cognitive function in post-cardiac rehabilitation patients BMC Complement Altern Med 14 411
del Zoppo G et al 2000 In1047298ammation and stroke putative role for cytokinesadhesion molecules and iNOS in brain response to ischemia Brain Pathol10 (1)95e112
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282282
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posttraumatic stress disorder Additionally recent models of neu-
roprogression suggest that the hippocampal atrophy observed in
unipolar depression is cumulative as the degree of atrophy appears
to be related to the number of untreated episodes and illness
duration (Sheline et al 2003 Berk et al 2011 Fries et al 2012)
One could therefore argue that the relationship between structural
brain abnormalities and affective disorders is bidirectional
The aetiology of depressive and anxious disorders are complex
and polygenetic and additional to structural abnormalities in-
dividuals show abnormalities in the function and expression of
monoamine neurotransmitters such as serotonin and dopamine
(Krishnan and Nestler 2008 Morilak and Frazer 2004) increased
oxidative stress (Michel et al 2012 Bouayed et al 2009) decreased
expression of the neurotropic protein brain-derived neurotrophic
factor (BDNF) (Autry and Monteggia 2012) and changes in the
expression of cytokines (Dantzer 2012) Cytokines are small cell
signalling protein molecules essential in the innate immune
response and in1047298ammation Cytokines can be either pro or anti-
in1047298ammatory (del Zoppo et al 2000) and among other functions
stimulate the autonomic nervous system (ANS) and the hypotha-
lamic pituitary adrenal (HPA) axis (Silverman and Sternberg 2012)
The ANS has two main divisions the parasympathetic nervous
system (PNS) and the sympathetic nervous system (SNS) TheSNS isinvolved in the mobilisation of the body in situations of stress to
either lsquo1047297ght or 1047298ightrsquo the stressor The PNS is responsible for
returning the body to a homoeostatic state after the activation of
the SNS (Buijs 2013) In many cases the PNS and SNS have com-
plementary and opposing actions in that one system is responsible
for activating a physiological response and the other is responsible
for inhibiting it (Buijs 2013) Activation of the SNS is associated
with a number of physiological changes including increased heart
rate blood pressure HPA axis activation and subsequent down-
stream release of the glucocorticoid hormone cortisol from the
adrenal cortex (Raison et al 2006) Glucocorticoid levels and the
further synthesis of pro-in1047298ammatory cytokines are normally
regulated by a HPA axis negative feedback mechanism (Silverman
and Sternberg 2012)The reciprocal relationship among stress HPA axis regulation
and depression and anxiety is well known (Dantzer 2012 Dantzer
et al 2008 Maes 2008a) Clinical depression and anxiety are
associated with an increased in1047298ammatory state These conditions
are characterized by dysfunctional glucocorticoid feedback inhibi-
tion (Silverman and Sternberg 2012) hypersecretion of CRH HPA
axis dysfunction (Boyer 2000 Roy-Byrne et al 1986) increased
circulatory cortisol (a widely used biomarker of HPA axis dysfunc-
tion) (Olson et al 2012) and production of pro-in1047298ammatory cy-
tokines (Silverman and Sternberg 2012 Raison et al 2006
Sapolsky et al 2000 King and Hegadoren 2002) Anxiety related
sustained central arousal has been proposed to deplete neuro-
transmission in the forebrain and thus precipitate the onset of
depression (Neale and Kendler 1995 Eison 1990 Johnson et al1990 Nutt et al 1998 Schulberg et al 1998)
On the other hand chronic stress and in1047298ammation can
contribute to the onset of depressive and anxious symptoms
(Dantzer 2012 Masi and Brovedani 2011 Pascoe et al 2011)
Treatment with the in1047298ammatory cytokine Interferon-a (INF-a)
(Capuron and Miller 2004) has been associated with the presen-
tation of depressive and anxious symptoms in cancer survivorships
(Capuron et al 2002) These depressive symptoms resolve with
INF-a therapy termination (Capuron and Dantzer 2003) and anti-
depressant medication (Musselman et al 2001)
Finally the bene1047297cial effects of pharmaceutical antidepressant
medications appear to relate to their in1047298uence on in1047298ammatory
activity Tricyclic antidepressant medications reduce pro-
in1047298
ammatory Interleukin-1 (IL-1) and Interleukin-2 (IL-2) and
increase anti-in1047298ammatory Interleukin-10 in animal models
(Kubera et al 2000) suggesting that these pharmaceutical anti-
depressant medications likely reduce depressive symptoms at
least in part by mediating mood modulating in1047298ammatory
markers (Kubera et al 2000) Additionally high basal in1047298amma-
tion is associated with a treatment resistance to pharmaceutical
anti-depressant interventions in clinical populations An
increased in1047298ammatory state as characterised by heightened
plasma concentrations of in1047298ammatory cytokines and acute phase
proteins prior to antidepressant treatment is associated with a
non-response (Maes 2008b Raison et al 2013)
Not only are current pharmacological treatment methods such
as selective serotonin reuptake inhibitors (SSRI) not bene1047297cial for
all individuals (Howland 2006 Kirsch et al 2008) these medica-
tions are associated with deleterious side effects such as metabolic
disorders and diabetes (McIntyre et al 2010) that reduce quality of
life and negatively in1047298uence individual adherence to the medica-
tion (Schatzberg 2007) Thus there is need for safer and more
effective treatment methods for mood disorders
12 Yoga is an effective treatment for depressive and anxious
symptomatology
The termyogais Sanskrit for lsquounionrsquo or lsquoto yokersquo and describes a
lifestyle aiming to achieve union of mind body and spirit While the
origins of yoga are unclear the Indian sage Patanjali described eight
limbs of yoga (G F 1998) which have been performed in Eastern
cultures for thousands of years In recent years yoga has become
increasingly popular in Western cultures (Ding and Stamatakis
2014 Tindle et al 2005) There are many forms of yoga each
with unique approaches and theoretical underpinnings making a
de1047297nitive taxonomy dif 1047297cult (Ospina et al 2007) Previous authors
have noted that this lack of a de1047297nitive de1047297nition and subsequent
differences in the forms studied has hampered neuroscienti1047297c
research in this 1047297eld (Lutz et al 2007) All forms of yoga however
share common elements including use of controlled breathing
(pranayama) physical postures (asanas) and meditative techniques(dhyana) to achieve well-being and mind body union and balance
(Farmer 2012 P1047298ueger 2011 Travis and Pearson 2000) Several
studies and systematic reviews demonstrate the mood enhancing
effects of yoga as treatments for clinical depression ( Uebelacker
et al 2010 Pilkington et al 2005 DSilva et al 2012
Balasubramaniam et al 2012) and anxiety (Chattha et al 2008
Granath et al 2006 Banerjee et al 2007 Harinath et al 2004
Kjellgren et al 2007 West et al 2004 Woolery et al 2004
Smith et al 2007 Li and Goldsmith 2012) Yoga practice is asso-
ciated with a reduced number of major depressive episodes and
lower risk for dysthymia which is a milder but longer-term form of
depression (Banerjee et al 2007 Kjellgren et al 2007 Woolery
et al 2004 John et al 2007 Sharma et al 2006 Butler et al
2008) Meta-analyses and systemic reviews indicate that yogaand meditative therapies are equally effective as conventional an-
tidepressants in the treatment of depressive and anxious disorders
(da Silva et al 2009 Cramer et al 2013 Chen et al 2012) The
limited data thus far suggests that these practices are associated
with changes in the stress response (Kinser et al 2012 McCall
2013) The neurobiological mechanisms however via which yoga
exerts its mood enhancing effects are still not clearly understood
2 Methods
21 Systematic search strategy
In the present study we aimed to systematically review rand-
omised control trials (RCTs) investigating the effects of yoga on
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 271
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stress-related biological measures and their neural correlates in
the context of depressive and anxious symptomology We searched
Pubmed MedlineOvid and Scopus with no year restriction for ar-
ticles containing the speci1047297c title word lsquoyogarsquo and the speci1047297c
abstract word lsquodepression rsquo lsquomoodrsquo lsquoanxietyrsquo lsquodepressive rsquo lsquoaffectiversquo
or lsquoanxiousrsquo and lsquoimmunersquo lsquocortisolrsquo lsquocatecholaminesrsquo lsquonorepi-
nephrinersquo lsquocytokinersquo lsquointerleukinrsquo lsquoInterferonrsquo lsquotumour necrosis
factor-alpharsquo lsquobrain-derived neurotropic factorrsquo lsquodopaminersquo lsquosero-
toninrsquo lsquoblood pressurersquo or lsquoheart ratersquo To explore the neural cor-
relates of stress in relation with yoga we searched the speci1047297c
abstract word lsquobrainrsquo and with the speci1047297c abstract words lsquomag-
netic resonance imaging (MRI)rsquo lsquofunctional MRIrsquo lsquodiffusion tensor
imaging (DTI)rsquo lsquoEEGrsquo lsquospectroscopyrsquo lsquoresting state fMRIrsquo lsquomagnetic
resonance spectroscopy (MRS)rsquo lsquopositron emission tomography
(PET)rsquo or lsquoarterial spin labelling (ASL)rsquo Articles reviewed were
restricted to original RCTs published in English that included a
population who engaged in a yoga practice with outcome mea-
sures related to HPA axis activation in1047298ammation or brain imaging
in conjunction with a measure of mood or current affective state
Review papers non-randomised trials case series and disserta-
tions were excluded
3 Results
A total of 122 papers with stress-related physiological parame-
ters were initially retrieved Studies were screened using title and
abstract when required full texts were accessed (n frac14 76) Nine of
these were excluded as they were review articles A further 31
papers were excluded as they were quasi-experimental cross
sectional of cohort studies four were excluded as they did not
include a biological and mood related outcome and 1047297ve were
excluded as they did not involve a yoga based intervention Three
additional papers were excluded as their results have not yet been
published Thus 24 RCT trials were included in the1047297nal review The
details of the search strategy are depicted in Fig 1
A total of 50 brain imaging papers were initially retrieved 34
were duplicates and were removed a further four were reviews
leaving 12 articles that were screened for eligibility seven were
removed as they did not include a brain imaging outcome one was
removed as it did not include a yoga asana intervention Three
further articles were removed as they were not RCTs Thus one RCT
trial was included in the 1047297nal review The details of the search
strategy are depicted in Fig 2
31 Characteristics of the included trials
Reviewed study characteristics are outlined in Table 1 Twenty-
1047297ve RCTs examining the effects of yoga on biological outcomes in
conjunction with mood related or brain related measures have
been included in this review Eight RCTs originated from India
(Sujatha and J A 2014 McDermott et al 2014 Kanojia et al 2013Ebnezar et al 2012 Gopal et al 2011 Telles et al 2010 Vadiraja
et al 2009 Malathi et al 1998) nine from the United States
(Woolery et al 2004 Corey et al 2014 Chandwani et al 2014
Kiecolt-Glaser et al 2014 Field et al 2013 Innes and Selfe
2012 Banasik et al 2011 Streeter et al 2010a) two from Australia
(Smith et al 2007 Cheema et al 2013) two from the United
Kingdom (Newham et al 2014 Bowden et al 2012) one from
Fig 1 Flow chart showing the retrieval process of biological related trials included in the systematic review
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282272
7262019 documento cientifico de la Yogapdf
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Germany (Sarubin et al 2014)onefrom Spain (Tolbanos Roche and
Mas Hesse 2014) one from Sweden (Hallgren et al 2014) and two
from Brazil (Danucalov et al 2013 Rocha et al 2012)
The studied populations were heterogeneous across trials three
involved individuals with depression (Woolery et al 2004 Fieldet al 2013 Sarubin et al 2014) one focused on healthy in-
dividuals experiencing mildmoderate stress (Smith et al 2007)
one studied individuals with alcohol dependence (Hallgren et al
2014) and one involved 1047298ood survivors (Telles et al 2010) Four
studied people with illnesses commonly comorbid to mood disor-
ders such as metabolic problems (McDermott et al 2014 Corey
et al 2014) and hypertension (Sujatha and J A 2014 Tolbanos
Roche and Mas Hesse 2014) Six trials focused on individuals
with medical conditions such as restless leg syndrome (Innes and
Selfe 2012) cancer survivorships (Vadiraja et al 2009
Chandwani et al 2014 Kiecolt-Glaser et al 2014 Banasik et al
2011) and osteoarthritis (Ebnezar et al 2012) One study involved
healthy military personal (Rocha et al 2012) Finally eight studies
involved healthy adults (Kanojia et al 2013 Gopal et al 2011Malathi et al 1998 Streeter et al 2010a Cheema et al 2013
Newham et al 2014 Bowden et al 2012) including familial
caregivers (Danucalov et al 2013)
Hatha yoga was the most common intervention and was used in
six trials (Smith et al 2007 Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Cheema et al 2013 Sarubin et al 2014 Danucalov
et al 2013) Iyengar yoga was the second most common inter-
vention and was used in 1047297ve trials (Woolery et al 2004 Innes and
Selfe 2012 Banasik et al 2011 Streeter et al 2010a Bowden et al
2012) while two trials used prenatal yoga (Field et al 2013
Newham et al 2014) One trial used restorative yoga (Corey et al
2014) one used Patanjali yoga (Telles et al 2010) four did not
specify the yoga form yet provided the sequence in the method-
ology (McDermott et al 2014 Kanojia et al 2013 Ebnezar et al
2012 Chandwani et al 2014) and six did not specify the yoga
form or clearly outline the sequence used (Gopal et al 2011
Vadiraja et al 2009 Malathi et al 1998 Tolbanos Roche and
Mas Hesse 2014 Hallgren et al 2014 Rocha et al 2012)
The most common stress-related biological measures (n frac14 11studies) were autonomic arousal measures including blood pres-
sure heartrate skinconductanceand respiration (Smithet al 2007
Sujatha and J A 2014 McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Gopal et al 2011 Telles et al 2010 Innes
and Selfe 2012 Tolbanos Roche and Mas Hesse 2014 Yeung et al
2014 Cheema et al 2013) Heart rate variability (HRV) was
measured in two studies as an indicator of ANS function and car-
diovascular response (Telles et al 2010 Cheema et al 2013)
increased HRV is interpreted to indicate greater parasympathetic
nervous system activity and a healthy balance between the sym-
pathetic and parasympathetic nervous systems (Buijs 2013)
The steroid hormone cortisol was assessed in 13 trials (Woolery
et al 2004 Gopal et al 2011 Vadiraja et al 2009 Corey et al
2014 Chandwani et al 2014 Field et al 2013 Banasik et al2011 Newham et al 2014 Bowden et al 2012 Sarubin et al
2014 Hallgren et al 2014 Danucalov et al 2013 Rocha et al
2012) Cytokines were measured in two trials (Gopal et al 2011
Kiecolt-Glaser et al 2014) Some other relevant health related
measures included lipid pro1047297les and body mass index (Sujatha and
J A 2014 McDermott et al 2014) As outlined in Table 1 all trials
included some measure of depressive symptoms except Sujatha
et al Smith et al Malathi et al and Ebnezar et al (Smith et al
2007 Sujatha and J A 2014 Ebnezar et al 2012 Malathi et al
1998) and 16 studies included a measure of anxiety (Woolery
et al 2004 Smith et al 2007 Sujatha and J A 2014 Ebnezar
et al 2012 Gopal et al 2011 Telles et al 2010 Vadiraja et al
2009 Field et al 2013 Innes and Selfe 2012 Streeter et al
2010a Cheema et al 2013 Newham et al 2014 Tolbanos Roche
Fig 2 Flow chart showing the retrieval process of imaging related trials included in the systematic review
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 273
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 513
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 613
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 713
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 813
and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
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more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Lutz A DJ Davidson RJ 2007 Meditation and the neuroscience of consciousnessIn Z P (Ed) Cambridge Handbook of Consciousness Cambridge University
Press Cambridge pp 499e
554Maes M 2008a The cytokine hypothesis of depression in1047298ammation oxidative amp
nitrosative stress (IOampNS) and leaky gut as new targets for adjunctive treat-ments in depression Neuroendocrinol Lett 29 (3) 287e291
Maes M 2008b The cytokine hypothesis of depression in1047298ammation oxidative ampnitrosative stress (IOampNS) and leaky gut as new targets for adjunctive treat-ments in depression Neuro Endocrinol Lett 29 (3) 287e291
Malathi A et al 1998 Psychophysiological changes at the time of examination inmedical students before and after the practice of yoga and relaxation Indian JPsychiatry 40 (1) 35e40
Masi G Brovedani P 2011 The hippocampus neurotrophic factors and depres-sion possible implications for the pharmacotherapy of depression CNS Drugs25 (11) 913e931
Mastorakos G Ilias I 2003 Maternal and fetal hypothalamic-pituitary-adrenalaxes during pregnancy and postpartum Ann N Y Acad Sci 997 136e149
Mathew AR et al 2011 Co-morbidity between major depressive disorder andanxiety disorders shared etiology or direct causation Psychol Med 41 (10)2023e2034
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 281
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1313
McCall MC 2013 How might yoga work an overview of potential underlyingmechanisms Yoga Phys Ther 3 (1)
McDermott KA et al 2014 A yoga intervention for type 2 diabetes risk reductiona pilot randomized controlled trial BMC Complement Altern Med 14 212
McEwen BS 2003 Mood disorders and allostatic load Biol Psychiatry 54 (3)200e207
McIntyre RS et al 2010 The association between conventional antidepressantsand the metabolic syndrome a review of the evidence and clinical implicationsCns Drugs 24 (9) 741e753
Michel TM Pulschen D Thome J 2012 The role of oxidative stress in depressive
disorders Curr Pharm Des 18 (36) 5890e
5899Miller EK Freedman DJ Wallis JD 2002 The prefrontal cortex categories
concepts and cognition Philos Trans R Soc Lond B Biol Sci 357 (1424)1123e1136
Morilak DA Frazer A 2004 Antidepressants and brain monoaminergic systemsa dimensional approach to understanding their behavioural effects in depres-sion and anxiety disorders Int J Neuropsychopharmacol 7 (2) 193e218
Musselman DL et al 2001 Paroxetine for the prevention of depression inducedby high-dose interferon alfa N Engl J Med 344 (13) 961e966
Neale MC Kendler KS 1995 Models of comorbidity for multifactorial disordersAm J Hum Genet 57 (4) 935e953
Nerurkar A et al 2011 When conventional medical providers recommend un-conventional medicine results of a national study Arch Intern Med 171 (9)862e864
Newham JJ et al 2014 Effects of antenatal yoga on maternal anxiety anddepression a randomized controlled trial Depress Anxiety 31 (8) 631e640
Nutt D Argyropoulos S F S 1998 Generalized Anxiety Disorder DiagnosisTreatment and its Relationship to Other Anxiety Disorders Martin Dunitz Ltd London
Olesen J et al 2012 The economic cost of brain disorders in Europe Eur J Neurol19 (1) 155e162
Olson KL Marc DT Grude LA McManus CJ Kellermann GH 2012 Thehypothalamic-pituitary-adrenal axis the actions of the Central Nervous Systemand Potential Biomarkers In Klatz R Goldman R (Eds) Anti-aging Thera-peutics vol XIII American Academy of Anti-Aging Medicine Chicago IL USApp 91e100 201
Organisation WH 2013 Depression FactsheetOspina MB et al 2007 Meditation practices for health state of the research Evid
Rep Technol Assess (Full Rep) (155) 1e263Pascoe MC et al 2011 In1047298ammation and depression why poststroke depression
may be the norm and not the exception Int J Stroke 6 (2) 128e135Penman S et al 2012 Yoga in Australia results of a national survey Int J Yoga 5
(2) 92e101P1047298ueger LW 2011 Yoga body the origins of modern posture practice Relig Stud
Rev 37 (3) 235e235Piet J Hougaard E 2011 The effect of mindfulness-based cognitive therapy for
prevention of relapse in recurrent major depressive disorder a systematic re-
view and meta-analysis Clin Psychol Rev 31 (6) 1032e
1040Pilkington K et al 2005 Yoga for depression the research evidence J AffectDisord 89 (1e3) 13e24
Poll EM et al 2007 Saliva collection method affects predictability of serumcortisol Clin Chim Acta 382 (1e2) 15e19
Raison CL et al 2013 A randomized controlled trial of the tumor necrosis factorantagonist in1047298iximab for treatment-resistant depression the role of baselinein1047298ammatory biomarkers JAMA Psychiatry 70 (1) 31e41
Raison CL Capuron L Miller AH 2006 Cytokines sing the blues in1047298ammationand the pathogenesis of depression Trends Immunol 27 (1) 24e31
Rocha KK et al 2012 Improvement in physiological and psychological parame-ters after 6 months of yoga practice Conscious Cogn 21 (2) 843e850
Roy-Byrne PP et al 1986 The corticotropin-releasing hormone stimulation test inpatients with panic disorder Am J Psychiatry 143 (7) 896e899
Sapolsky RM Romero LM Munck AU 2000 How do glucocorticoids in1047298uencestress responses Integrating permissive suppressive stimulatory and pre-parative actions Endocr Rev 21 (1) 55e89
Sarubin N et al 2014 The in1047298uence of Hatha yoga as an add-on treatment inmajor depression on hypothalamic-pituitary-adrenal-axis activity a random-
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83Schatzberg AF 2007 Safety and tolerability of antidepressants weighing the
impact on treatment decisions J Clin Psychiatry 68 (Suppl 8) 26e34Schulberg HC Katon WJ S MK 1998 Management of mood and anxiety dis-
orders in primary care In Rush AJ (Ed) Mood and Anxiety Disorders CurrentScience Inc Philadelphia PA
Sharma VK et al 2006 Effect of Sahaj Yoga on neuro-cognitive functions in pa-tients suffering from major depression Indian J Physiol Pharmacol 50 (4)375e383
Sheline YI Gado MH Kraemer HC 2003 Untreated depression and hippo-campal volume loss Am J Psychiatry 160 (8) 1516e1518
Shyn SI Hamilton SP 2010 The genetics of major depression moving beyondthe monoamine hypothesis Psychiatr Clin North Am 33 (1) 125e140
Siegle GJ et al 2002 Cant shake that feeling assessment of sustained event-related fMRI amygdala activity in response to emotional information indepressed individuals Biol Psychiatry 51 (9) 693e707
da Silva TL Ravindran LN Ravindran AV 2009 Yoga in the treatment of moodand anxiety disorders a review Asian J Psychiatr 2 (1) 6e16
Silverman MN Sternberg EM 2012 Glucocorticoid regulation of in1047298ammationand its functional correlates from HPA axis to glucocorticoid receptordysfunction Ann N Y Acad Sci 1261 55e63
Smith C et al 2007 A randomised comparative trial of yoga and relaxation toreduce stress and anxiety Complement Ther Med 15 (2) 77e83
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern Complement Med16 (11) 1145e1152
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern ComplementaryMed 16 (11) 1145e1152
Streeter CC et al 2012 Effects of yoga on the autonomic nervous system gamma-aminobutyric-acid and allostasis in epilepsy depression and post-traumaticstress disorder Med Hypotheses 78 (5) 571e579
Sujatha T J A 2014 Efectivenes of a 12-Wek yoga program on physiopsychologicalparameters in patients with hypertension Int J Pharm Clin Res 6 (4)329e335
Telles S et al 2010 Post traumatic stress symptoms and heart rate variability inBihar 1047298ood survivors following yoga a randomized controlled study BMCPsychiatry 10 18
Tindle HA et al 2005 Trends in use of complementary and alternative medicineby us adults 1997-2002 Altern Ther Health Med 11 (1) 42e49
Tolbanos Roche L Mas Hesse B 2014 Application of an integrative yoga therapyprogramme in cases of essential arterial hypertension in public healthcareComplement Ther Clin Pract 20 (4) 285e290 httpdxdoiorg101016
jctcp201410004Travis F Pearson C 200 0 Pure consciousness distinct phenomenological and
physiological correlates of ldquoconsciousness itself rdquo Int J Neurosci 100 (1e4)77e89
Uebelacker LA et al 2010 Hatha yoga for depression critical review of the evi-dence for ef 1047297cacy plausible mechanisms of action and directions for futureresearch J Psychiatr Pract 16 (1) 22e33
Vadiraja HS et al 2009 Effects of a yoga program on cortisol rhythm and moodstates in early breast cancer patients undergoing adjuvant radiotherapy arandomized controlled trial Integr Cancer Ther 8 (1) 37e46
Wardle J Adams J Sibbritt D 2014 Referral to yoga therapists in rural primaryhealth care a survey of general practitioners in rural and regional New SouthWales Australia Int J Yoga 7 (1) 9e16
Weibel L 2003 Methodological guidelines for the use of salivary cortisol as bio-logical marker of stress Presse Med 32 (18) 845e851
West J et al 2004 Effects of Hatha yoga and African dance on perceived stressaffect and salivary cortisol Ann Behav Med 28 (2) 114e118
Whiteford HA et al 2013 Global burden of disease attributable to mental andsubstance use disorders 1047297ndings from the global Burden of Disease Study 2010Lancet 382 (9904) 1575e1586
Wittchen HU et al 2011 The size and burden of mental disorders and otherdisorders of the brain in Europe 2010 Eur Neuropsychopharmacol 21 (9)655e679
Woolery A et al 2004 A yoga intervention for young adults with elevatedsymptoms of depression Altern Ther Health Med 10 (2) 60e63
Yang Y Raine A 2009 Prefrontal structural and functional brain imaging 1047297ndingsin antisocial violent and psychopathic individuals a meta-analysis PsychiatryRes 174 (2) 81e88
Yeung A et al 2014 Randomised controlled trial of a 12 week yoga intervention
on negative affective states cardiovascular and cognitive function in post-cardiac rehabilitation patients BMC Complement Altern Med 14 411
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MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282282
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stress-related biological measures and their neural correlates in
the context of depressive and anxious symptomology We searched
Pubmed MedlineOvid and Scopus with no year restriction for ar-
ticles containing the speci1047297c title word lsquoyogarsquo and the speci1047297c
abstract word lsquodepression rsquo lsquomoodrsquo lsquoanxietyrsquo lsquodepressive rsquo lsquoaffectiversquo
or lsquoanxiousrsquo and lsquoimmunersquo lsquocortisolrsquo lsquocatecholaminesrsquo lsquonorepi-
nephrinersquo lsquocytokinersquo lsquointerleukinrsquo lsquoInterferonrsquo lsquotumour necrosis
factor-alpharsquo lsquobrain-derived neurotropic factorrsquo lsquodopaminersquo lsquosero-
toninrsquo lsquoblood pressurersquo or lsquoheart ratersquo To explore the neural cor-
relates of stress in relation with yoga we searched the speci1047297c
abstract word lsquobrainrsquo and with the speci1047297c abstract words lsquomag-
netic resonance imaging (MRI)rsquo lsquofunctional MRIrsquo lsquodiffusion tensor
imaging (DTI)rsquo lsquoEEGrsquo lsquospectroscopyrsquo lsquoresting state fMRIrsquo lsquomagnetic
resonance spectroscopy (MRS)rsquo lsquopositron emission tomography
(PET)rsquo or lsquoarterial spin labelling (ASL)rsquo Articles reviewed were
restricted to original RCTs published in English that included a
population who engaged in a yoga practice with outcome mea-
sures related to HPA axis activation in1047298ammation or brain imaging
in conjunction with a measure of mood or current affective state
Review papers non-randomised trials case series and disserta-
tions were excluded
3 Results
A total of 122 papers with stress-related physiological parame-
ters were initially retrieved Studies were screened using title and
abstract when required full texts were accessed (n frac14 76) Nine of
these were excluded as they were review articles A further 31
papers were excluded as they were quasi-experimental cross
sectional of cohort studies four were excluded as they did not
include a biological and mood related outcome and 1047297ve were
excluded as they did not involve a yoga based intervention Three
additional papers were excluded as their results have not yet been
published Thus 24 RCT trials were included in the1047297nal review The
details of the search strategy are depicted in Fig 1
A total of 50 brain imaging papers were initially retrieved 34
were duplicates and were removed a further four were reviews
leaving 12 articles that were screened for eligibility seven were
removed as they did not include a brain imaging outcome one was
removed as it did not include a yoga asana intervention Three
further articles were removed as they were not RCTs Thus one RCT
trial was included in the 1047297nal review The details of the search
strategy are depicted in Fig 2
31 Characteristics of the included trials
Reviewed study characteristics are outlined in Table 1 Twenty-
1047297ve RCTs examining the effects of yoga on biological outcomes in
conjunction with mood related or brain related measures have
been included in this review Eight RCTs originated from India
(Sujatha and J A 2014 McDermott et al 2014 Kanojia et al 2013Ebnezar et al 2012 Gopal et al 2011 Telles et al 2010 Vadiraja
et al 2009 Malathi et al 1998) nine from the United States
(Woolery et al 2004 Corey et al 2014 Chandwani et al 2014
Kiecolt-Glaser et al 2014 Field et al 2013 Innes and Selfe
2012 Banasik et al 2011 Streeter et al 2010a) two from Australia
(Smith et al 2007 Cheema et al 2013) two from the United
Kingdom (Newham et al 2014 Bowden et al 2012) one from
Fig 1 Flow chart showing the retrieval process of biological related trials included in the systematic review
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282272
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Germany (Sarubin et al 2014)onefrom Spain (Tolbanos Roche and
Mas Hesse 2014) one from Sweden (Hallgren et al 2014) and two
from Brazil (Danucalov et al 2013 Rocha et al 2012)
The studied populations were heterogeneous across trials three
involved individuals with depression (Woolery et al 2004 Fieldet al 2013 Sarubin et al 2014) one focused on healthy in-
dividuals experiencing mildmoderate stress (Smith et al 2007)
one studied individuals with alcohol dependence (Hallgren et al
2014) and one involved 1047298ood survivors (Telles et al 2010) Four
studied people with illnesses commonly comorbid to mood disor-
ders such as metabolic problems (McDermott et al 2014 Corey
et al 2014) and hypertension (Sujatha and J A 2014 Tolbanos
Roche and Mas Hesse 2014) Six trials focused on individuals
with medical conditions such as restless leg syndrome (Innes and
Selfe 2012) cancer survivorships (Vadiraja et al 2009
Chandwani et al 2014 Kiecolt-Glaser et al 2014 Banasik et al
2011) and osteoarthritis (Ebnezar et al 2012) One study involved
healthy military personal (Rocha et al 2012) Finally eight studies
involved healthy adults (Kanojia et al 2013 Gopal et al 2011Malathi et al 1998 Streeter et al 2010a Cheema et al 2013
Newham et al 2014 Bowden et al 2012) including familial
caregivers (Danucalov et al 2013)
Hatha yoga was the most common intervention and was used in
six trials (Smith et al 2007 Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Cheema et al 2013 Sarubin et al 2014 Danucalov
et al 2013) Iyengar yoga was the second most common inter-
vention and was used in 1047297ve trials (Woolery et al 2004 Innes and
Selfe 2012 Banasik et al 2011 Streeter et al 2010a Bowden et al
2012) while two trials used prenatal yoga (Field et al 2013
Newham et al 2014) One trial used restorative yoga (Corey et al
2014) one used Patanjali yoga (Telles et al 2010) four did not
specify the yoga form yet provided the sequence in the method-
ology (McDermott et al 2014 Kanojia et al 2013 Ebnezar et al
2012 Chandwani et al 2014) and six did not specify the yoga
form or clearly outline the sequence used (Gopal et al 2011
Vadiraja et al 2009 Malathi et al 1998 Tolbanos Roche and
Mas Hesse 2014 Hallgren et al 2014 Rocha et al 2012)
The most common stress-related biological measures (n frac14 11studies) were autonomic arousal measures including blood pres-
sure heartrate skinconductanceand respiration (Smithet al 2007
Sujatha and J A 2014 McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Gopal et al 2011 Telles et al 2010 Innes
and Selfe 2012 Tolbanos Roche and Mas Hesse 2014 Yeung et al
2014 Cheema et al 2013) Heart rate variability (HRV) was
measured in two studies as an indicator of ANS function and car-
diovascular response (Telles et al 2010 Cheema et al 2013)
increased HRV is interpreted to indicate greater parasympathetic
nervous system activity and a healthy balance between the sym-
pathetic and parasympathetic nervous systems (Buijs 2013)
The steroid hormone cortisol was assessed in 13 trials (Woolery
et al 2004 Gopal et al 2011 Vadiraja et al 2009 Corey et al
2014 Chandwani et al 2014 Field et al 2013 Banasik et al2011 Newham et al 2014 Bowden et al 2012 Sarubin et al
2014 Hallgren et al 2014 Danucalov et al 2013 Rocha et al
2012) Cytokines were measured in two trials (Gopal et al 2011
Kiecolt-Glaser et al 2014) Some other relevant health related
measures included lipid pro1047297les and body mass index (Sujatha and
J A 2014 McDermott et al 2014) As outlined in Table 1 all trials
included some measure of depressive symptoms except Sujatha
et al Smith et al Malathi et al and Ebnezar et al (Smith et al
2007 Sujatha and J A 2014 Ebnezar et al 2012 Malathi et al
1998) and 16 studies included a measure of anxiety (Woolery
et al 2004 Smith et al 2007 Sujatha and J A 2014 Ebnezar
et al 2012 Gopal et al 2011 Telles et al 2010 Vadiraja et al
2009 Field et al 2013 Innes and Selfe 2012 Streeter et al
2010a Cheema et al 2013 Newham et al 2014 Tolbanos Roche
Fig 2 Flow chart showing the retrieval process of imaging related trials included in the systematic review
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 273
7262019 documento cientifico de la Yogapdf
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7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 613
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 713
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and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 277
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 913
condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 279
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more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Roy-Byrne PP et al 1986 The corticotropin-releasing hormone stimulation test inpatients with panic disorder Am J Psychiatry 143 (7) 896e899
Sapolsky RM Romero LM Munck AU 2000 How do glucocorticoids in1047298uencestress responses Integrating permissive suppressive stimulatory and pre-parative actions Endocr Rev 21 (1) 55e89
Sarubin N et al 2014 The in1047298uence of Hatha yoga as an add-on treatment inmajor depression on hypothalamic-pituitary-adrenal-axis activity a random-
ized trial J Psychiatr Res 53 76e
83Schatzberg AF 2007 Safety and tolerability of antidepressants weighing the
impact on treatment decisions J Clin Psychiatry 68 (Suppl 8) 26e34Schulberg HC Katon WJ S MK 1998 Management of mood and anxiety dis-
orders in primary care In Rush AJ (Ed) Mood and Anxiety Disorders CurrentScience Inc Philadelphia PA
Sharma VK et al 2006 Effect of Sahaj Yoga on neuro-cognitive functions in pa-tients suffering from major depression Indian J Physiol Pharmacol 50 (4)375e383
Sheline YI Gado MH Kraemer HC 2003 Untreated depression and hippo-campal volume loss Am J Psychiatry 160 (8) 1516e1518
Shyn SI Hamilton SP 2010 The genetics of major depression moving beyondthe monoamine hypothesis Psychiatr Clin North Am 33 (1) 125e140
Siegle GJ et al 2002 Cant shake that feeling assessment of sustained event-related fMRI amygdala activity in response to emotional information indepressed individuals Biol Psychiatry 51 (9) 693e707
da Silva TL Ravindran LN Ravindran AV 2009 Yoga in the treatment of moodand anxiety disorders a review Asian J Psychiatr 2 (1) 6e16
Silverman MN Sternberg EM 2012 Glucocorticoid regulation of in1047298ammationand its functional correlates from HPA axis to glucocorticoid receptordysfunction Ann N Y Acad Sci 1261 55e63
Smith C et al 2007 A randomised comparative trial of yoga and relaxation toreduce stress and anxiety Complement Ther Med 15 (2) 77e83
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern Complement Med16 (11) 1145e1152
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern ComplementaryMed 16 (11) 1145e1152
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Telles S et al 2010 Post traumatic stress symptoms and heart rate variability inBihar 1047298ood survivors following yoga a randomized controlled study BMCPsychiatry 10 18
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Tolbanos Roche L Mas Hesse B 2014 Application of an integrative yoga therapyprogramme in cases of essential arterial hypertension in public healthcareComplement Ther Clin Pract 20 (4) 285e290 httpdxdoiorg101016
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physiological correlates of ldquoconsciousness itself rdquo Int J Neurosci 100 (1e4)77e89
Uebelacker LA et al 2010 Hatha yoga for depression critical review of the evi-dence for ef 1047297cacy plausible mechanisms of action and directions for futureresearch J Psychiatr Pract 16 (1) 22e33
Vadiraja HS et al 2009 Effects of a yoga program on cortisol rhythm and moodstates in early breast cancer patients undergoing adjuvant radiotherapy arandomized controlled trial Integr Cancer Ther 8 (1) 37e46
Wardle J Adams J Sibbritt D 2014 Referral to yoga therapists in rural primaryhealth care a survey of general practitioners in rural and regional New SouthWales Australia Int J Yoga 7 (1) 9e16
Weibel L 2003 Methodological guidelines for the use of salivary cortisol as bio-logical marker of stress Presse Med 32 (18) 845e851
West J et al 2004 Effects of Hatha yoga and African dance on perceived stressaffect and salivary cortisol Ann Behav Med 28 (2) 114e118
Whiteford HA et al 2013 Global burden of disease attributable to mental andsubstance use disorders 1047297ndings from the global Burden of Disease Study 2010Lancet 382 (9904) 1575e1586
Wittchen HU et al 2011 The size and burden of mental disorders and otherdisorders of the brain in Europe 2010 Eur Neuropsychopharmacol 21 (9)655e679
Woolery A et al 2004 A yoga intervention for young adults with elevatedsymptoms of depression Altern Ther Health Med 10 (2) 60e63
Yang Y Raine A 2009 Prefrontal structural and functional brain imaging 1047297ndingsin antisocial violent and psychopathic individuals a meta-analysis PsychiatryRes 174 (2) 81e88
Yeung A et al 2014 Randomised controlled trial of a 12 week yoga intervention
on negative affective states cardiovascular and cognitive function in post-cardiac rehabilitation patients BMC Complement Altern Med 14 411
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Germany (Sarubin et al 2014)onefrom Spain (Tolbanos Roche and
Mas Hesse 2014) one from Sweden (Hallgren et al 2014) and two
from Brazil (Danucalov et al 2013 Rocha et al 2012)
The studied populations were heterogeneous across trials three
involved individuals with depression (Woolery et al 2004 Fieldet al 2013 Sarubin et al 2014) one focused on healthy in-
dividuals experiencing mildmoderate stress (Smith et al 2007)
one studied individuals with alcohol dependence (Hallgren et al
2014) and one involved 1047298ood survivors (Telles et al 2010) Four
studied people with illnesses commonly comorbid to mood disor-
ders such as metabolic problems (McDermott et al 2014 Corey
et al 2014) and hypertension (Sujatha and J A 2014 Tolbanos
Roche and Mas Hesse 2014) Six trials focused on individuals
with medical conditions such as restless leg syndrome (Innes and
Selfe 2012) cancer survivorships (Vadiraja et al 2009
Chandwani et al 2014 Kiecolt-Glaser et al 2014 Banasik et al
2011) and osteoarthritis (Ebnezar et al 2012) One study involved
healthy military personal (Rocha et al 2012) Finally eight studies
involved healthy adults (Kanojia et al 2013 Gopal et al 2011Malathi et al 1998 Streeter et al 2010a Cheema et al 2013
Newham et al 2014 Bowden et al 2012) including familial
caregivers (Danucalov et al 2013)
Hatha yoga was the most common intervention and was used in
six trials (Smith et al 2007 Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Cheema et al 2013 Sarubin et al 2014 Danucalov
et al 2013) Iyengar yoga was the second most common inter-
vention and was used in 1047297ve trials (Woolery et al 2004 Innes and
Selfe 2012 Banasik et al 2011 Streeter et al 2010a Bowden et al
2012) while two trials used prenatal yoga (Field et al 2013
Newham et al 2014) One trial used restorative yoga (Corey et al
2014) one used Patanjali yoga (Telles et al 2010) four did not
specify the yoga form yet provided the sequence in the method-
ology (McDermott et al 2014 Kanojia et al 2013 Ebnezar et al
2012 Chandwani et al 2014) and six did not specify the yoga
form or clearly outline the sequence used (Gopal et al 2011
Vadiraja et al 2009 Malathi et al 1998 Tolbanos Roche and
Mas Hesse 2014 Hallgren et al 2014 Rocha et al 2012)
The most common stress-related biological measures (n frac14 11studies) were autonomic arousal measures including blood pres-
sure heartrate skinconductanceand respiration (Smithet al 2007
Sujatha and J A 2014 McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Gopal et al 2011 Telles et al 2010 Innes
and Selfe 2012 Tolbanos Roche and Mas Hesse 2014 Yeung et al
2014 Cheema et al 2013) Heart rate variability (HRV) was
measured in two studies as an indicator of ANS function and car-
diovascular response (Telles et al 2010 Cheema et al 2013)
increased HRV is interpreted to indicate greater parasympathetic
nervous system activity and a healthy balance between the sym-
pathetic and parasympathetic nervous systems (Buijs 2013)
The steroid hormone cortisol was assessed in 13 trials (Woolery
et al 2004 Gopal et al 2011 Vadiraja et al 2009 Corey et al
2014 Chandwani et al 2014 Field et al 2013 Banasik et al2011 Newham et al 2014 Bowden et al 2012 Sarubin et al
2014 Hallgren et al 2014 Danucalov et al 2013 Rocha et al
2012) Cytokines were measured in two trials (Gopal et al 2011
Kiecolt-Glaser et al 2014) Some other relevant health related
measures included lipid pro1047297les and body mass index (Sujatha and
J A 2014 McDermott et al 2014) As outlined in Table 1 all trials
included some measure of depressive symptoms except Sujatha
et al Smith et al Malathi et al and Ebnezar et al (Smith et al
2007 Sujatha and J A 2014 Ebnezar et al 2012 Malathi et al
1998) and 16 studies included a measure of anxiety (Woolery
et al 2004 Smith et al 2007 Sujatha and J A 2014 Ebnezar
et al 2012 Gopal et al 2011 Telles et al 2010 Vadiraja et al
2009 Field et al 2013 Innes and Selfe 2012 Streeter et al
2010a Cheema et al 2013 Newham et al 2014 Tolbanos Roche
Fig 2 Flow chart showing the retrieval process of imaging related trials included in the systematic review
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and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 279
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1113
more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
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more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Hallgren M et al 2014 Yoga as an adjunct treatment for alcohol dependence apilot study Complement Ther Med 22 (3) 441e445
Harinath K et al 2004 Effects of Hatha yoga and Omkar meditation on cardio-respiratory performance psychologic pro1047297le and melatonin secretion J AlternComplement Med 10 (2) 261e268
Hariprasad VR et al 2013 Yoga increases the volume of the hippocampus inelderly subjects Indian J Psychiatry 55 (Suppl 3) S394eS396
Herman JP et al 2005 Limbic system mechanisms of stress regulationhypothalamo-pituitary-adrenocortical axis Prog Neuropsychopharmacol BiolPsychiatry 29 (8) 1201e1213
Howland RH 2006 Pharmacotherapy strategies for treatment-resistant depres-sion J Psychosoc Nurs Ment Health Serv 44 (11) 11e14
Hranov LG 2007 Comorbid anxiety and depression illumination of a controversyInt J Psychiatry Clin Pract 11 (3) 171e189
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Ionescu DF et al 2013 Neurobiology of anxious depression a review DepressAnxiety 30 (4) 374e385
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John PJ et al 2007 Effectiveness of yoga therapy in the treatment of migrainewithout aura a randomized controlled trial Headache 47 (5) 654e661
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and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 279
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1113
more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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on negative affective states cardiovascular and cognitive function in post-cardiac rehabilitation patients BMC Complement Altern Med 14 411
del Zoppo G et al 2000 In1047298ammation and stroke putative role for cytokinesadhesion molecules and iNOS in brain response to ischemia Brain Pathol10 (1)95e112
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and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
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more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282282
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and Mas Hesse 2014 Hallgren et al 2014 Danucalov et al 2013
Rocha et al 2012) Other studied measures included quality of life
(Smith et al 2007 Chandwani et al 2014 Kiecolt-Glaser et al
2014 Cheema et al 2013) stress or perceived stress (Sujatha and J
A 2014 McDermott et al 2014 Vadiraja et al 2009 Corey et al
2014 Innes and Selfe 2012 Hallgren et al 2014 Danucalov
et al 2013 Rocha et al 2012) fatigue and sleep quality (Telles
et al 2010 Chandwani et al 2014 Kiecolt-Glaser et al 2014
Innes and Selfe 2012 Bowden et al 2012) and pain or disability
(Smith et al 2007 Ebnezar et al 2012 Banasik et al 2011)
32 Findings of the included trials
321 Cortisol outcomes
Many of the reviewed studies assessed salivary cortisol There
are some limitations associated with salivary cortisol measure-
ments that can affect the reliability of the outcome Various drugs
and medications including caffeine pharmaceutical anti-
depressants and over-the-counter hydrocortisone creams affect
cortisol levels (Poll et al 2007 Granger et al 2009) as well as
smoking (Badrick et al 2007) and blood in the saliva (Ashman
et al 2002) Eating and drinking substances with low pH can
arti1047297cially increase cortisol levels (Goodyer et al 1996) and homecollection can be associated with compliance issues deviation from
instructions as well as insuf 1047297cient provision of saliva (Weibel
2003) Thus in clinical research it is important to ensure that
salivary measures are taken at several repeated measures over the
course of several days at the same time intervals Additionally as
cortisol levels follow a circadian rhythm the time of day that
cortisol sampling occurs should be held constant across the inter-
vention Controlling for waking time when assessing the cortisol
awakening response (CAR) (which is characterised by a rise in
cortisol upon awakening generally reaching its peak during the
initial 30e45 min after waking (Clow et al 2004)) is also important
(Clow et al 2004) Early waking time has been associated with
heightened CAR (Kudielka and Kirschbaum 2003) Thus waking
time should be documented and explored as a possible confound-ing factor The above collection conditions were satis1047297ed in most of
the reviewed studies as shown in Table 1 Those studies that did not
satisfy the above discussed collection standards of salivary cortisol
are discussed below where relevant
322 Salivary cortisol before and following yoga classes
Only two studies measured salivary cortisol before and
following yoga classes Newham et al found that eight weeks of
prenatal yoga was associated with decreased salivary cortisol state
anxiety and pregnancy speci1047297c anxiety in healthy women
compared to treatment as usual both after the 1047297rst yoga class and
after the 1047297nal yoga class (Newham et al 2014) Similarly in a trial
by Field et al involving 96 women with prenatal depression one
session of prenatal yoga was seen to decrease depression anxietyanger and pain After 12 weeks of yoga decreases were also
observed in cortisol estriol and progesterone Effects were also
seen after 12 weeks of a social support group suggesting a role of
social support in mediating HPA activity (Field et al 2013) The
authors state that the time of cortisol estriol and progesterone
sampling was held constant across the yoga intervention as sam-
ples were taken at mid morning both pre and post intervention
(Field et al 2013) Thus these two studies indicate that yoga
practice appears to have an immediate bene1047297cial effect on cortisol
levels
323 Daytime cortisol
Two studies measured daytime cortisol Bowden et al tested
fasting (2 h) salivary cortisol in healthy adults and found that
Iyenger yoga Brain Wave Vibration (a meditation practised in a
class involving rhythmic movements of the head neck and body)
and mindfulness classes were not associated with a change in
cortisol All interventions however improved mindfulness and
decreasedmeasures of stress A limitation of this study is that saliva
samples for cortisol testing were collected between 11am and 3pm
so the exact time of collection was not held constant between all
participants The authors highlighted however that cortisol levels
are relatively stable between these times that two separate sam-
ples from each individual were taken at each time point and that
pre-post intervention collection times for each individuals were
matched (Bowden et al 2012)
Banasik et al found that eight weeks of Iyengar yoga practice
was associated with lower salivary cortisol collected at 1047297ve pm
among breast cancer survivors (Banasik et al 2011) These authors
however did not specify if participants were fasting or not before
cortisol collection and as previously stated eating and drinking
various substances can arti1047297cially affect cortisol levels thus these
1047297ndings should be interpreted with caution (Goodyer et al 1996)
Given the limited evidence thus far and the possible methodolog-
ical shortcomings of the study by Banasik et al it is unclear at this
stage if yoga practice affects daytime cortisol
324 Waking and bedtime salivary cortisol
Findings of the effects of yoga classes on waking cortisol levels
are mixed Danucalov et al reported that hatha yoga in conjunction
with compassion meditation was associated with decreased sali-
vary waking cortisol depression anxiety and stress when prac-
ticed for eight weeks in familial caregivers as compared to a non-
treatment control group (Danucalov et al 2013) Banasik et al
also found that eight weeks of Iyengar yoga practice was associated
with lower morning cortisol and better emotional well-being
among breast cancer survivors Participants recorded the time of
collection on tracking forms with 95 of collections occurring
within 20 min of the assigned times and cortisol samples were
collected over two consecutive days at each time point in this study
(Banasik et al 2011) Chandwani et al found that in patients withbreast cancer a six-week yoga program involving a range of
physical yoga asanas was associated with a steeper cortisol slope
and decreased fatigue compared to individuals in a stretching or
waitlist control group at the end of radiotherapy A limitation of
this study is that the particular wake up time of individual partic-
ipants was not controlled for however samples were taken at the
same time intervals after waking for three consecutive days at each
time point (Chandwani et al 2014) and CAR has been shown to be
relativity stabile across consecutive days (Edwards et al 2001) In
another group of 56 patients with breast cancer Vadiraja et al
demonstrated that six weeks of yoga decreased waking and
bedtime salivary cortisol which corresponded to reduced depres-
sion anxiety and perceived stress as compared to brief supportive
therapy It should be noted that the brief supportive therapy groupreceived three-four 15 min individual counselling sessions during
six weeks whereas the yoga group received 18e24 yoga sessions
(Vadiraja et al 2009) Rocha et al found that six months of yoga
plus physical exercise was associated with decreased waking
cortisol depression anxiety and stress compared to exercise alone
among male Brazilian military personal However this study only
took a single waking cortisol measure at each collection time point
(Rocha et al 2012)
Contrarily Corey et al observed that after six month of
stretching or restorative yoga classes individuals in the stretching
conditions showed reduced waking and bedtime cortisol and had
lower self-perceived stress ratings than those in the restorative
yoga group Notably in the stretching condition poses were
changed approximately every 30s while in the restorative yoga
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 277
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 279
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more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Silverman MN Sternberg EM 2012 Glucocorticoid regulation of in1047298ammationand its functional correlates from HPA axis to glucocorticoid receptordysfunction Ann N Y Acad Sci 1261 55e63
Smith C et al 2007 A randomised comparative trial of yoga and relaxation toreduce stress and anxiety Complement Ther Med 15 (2) 77e83
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern Complement Med16 (11) 1145e1152
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern ComplementaryMed 16 (11) 1145e1152
Streeter CC et al 2012 Effects of yoga on the autonomic nervous system gamma-aminobutyric-acid and allostasis in epilepsy depression and post-traumaticstress disorder Med Hypotheses 78 (5) 571e579
Sujatha T J A 2014 Efectivenes of a 12-Wek yoga program on physiopsychologicalparameters in patients with hypertension Int J Pharm Clin Res 6 (4)329e335
Telles S et al 2010 Post traumatic stress symptoms and heart rate variability inBihar 1047298ood survivors following yoga a randomized controlled study BMCPsychiatry 10 18
Tindle HA et al 2005 Trends in use of complementary and alternative medicineby us adults 1997-2002 Altern Ther Health Med 11 (1) 42e49
Tolbanos Roche L Mas Hesse B 2014 Application of an integrative yoga therapyprogramme in cases of essential arterial hypertension in public healthcareComplement Ther Clin Pract 20 (4) 285e290 httpdxdoiorg101016
jctcp201410004Travis F Pearson C 200 0 Pure consciousness distinct phenomenological and
physiological correlates of ldquoconsciousness itself rdquo Int J Neurosci 100 (1e4)77e89
Uebelacker LA et al 2010 Hatha yoga for depression critical review of the evi-dence for ef 1047297cacy plausible mechanisms of action and directions for futureresearch J Psychiatr Pract 16 (1) 22e33
Vadiraja HS et al 2009 Effects of a yoga program on cortisol rhythm and moodstates in early breast cancer patients undergoing adjuvant radiotherapy arandomized controlled trial Integr Cancer Ther 8 (1) 37e46
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Weibel L 2003 Methodological guidelines for the use of salivary cortisol as bio-logical marker of stress Presse Med 32 (18) 845e851
West J et al 2004 Effects of Hatha yoga and African dance on perceived stressaffect and salivary cortisol Ann Behav Med 28 (2) 114e118
Whiteford HA et al 2013 Global burden of disease attributable to mental andsubstance use disorders 1047297ndings from the global Burden of Disease Study 2010Lancet 382 (9904) 1575e1586
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Woolery A et al 2004 A yoga intervention for young adults with elevatedsymptoms of depression Altern Ther Health Med 10 (2) 60e63
Yang Y Raine A 2009 Prefrontal structural and functional brain imaging 1047297ndingsin antisocial violent and psychopathic individuals a meta-analysis PsychiatryRes 174 (2) 81e88
Yeung A et al 2014 Randomised controlled trial of a 12 week yoga intervention
on negative affective states cardiovascular and cognitive function in post-cardiac rehabilitation patients BMC Complement Altern Med 14 411
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condition they were changed every 10e15min The authors spec-
ulated that these results might be due to increased physical activity
in the stretching condition This hypothesis is inconsistent with the
above-discussed 1047297ndings of Rocha et al who reported that yoga
plus exercise was more effective than exercise alone at lowering
cortisol levels (Rocha et al 2012) Alternatively post hoc analysis in
the study by Corey et al showed that increased perceived social
support in the stretching group was related to changes in cortisol
In the stretching intervention individuals partook in weekly dis-
cussion while in the restorative yoga group communication be-
tween participants was minimal (Corey et al 2014) These results
indicate that physical practices that incorporate a social aspect may
be more effective in modulating HPA activity Participants in this
study were asked to collect their morning cortisol sample before
11am so exact time of collection was not held constant between all
participants however 4 samplesday for three consecutive days
were collected from each participant at each time point the au-
thors found no signi1047297cant variance across the three test days and
the 1047297nal cortisol measure was averaged over the three days (Corey
et al 2014)
A pilot RCT by Hallgren et al involving 18-alcohol dependent
individuals showed that a 10-week yoga program was associated
with a non-signi1047297cant reduction in morning cortisol and alcoholconsumption at six months The authors speculated that the small
sample size might explain the absences of a signi1047297cant effect A
methodological limitation of this study is that individuals were not
tested upon completion of the yoga intervention but instead at six
months approximately three months after the completion of the
program Additionally no information was provided regarding the
time of day for cortisol collection or if multiple samples were
collected and thus this study appears to lack methodological rigour
(Hallgren et al 2014) In a small study involving 28 university
students experiencing mildmoderate depression Woolery et al
reported that 1047297ve weeks of Iyengar yoga decreased depression and
anxiety scores however there was only a trend for higher morning
cortisol In this study however only one salivary sample (waking
cortisol) was taken at each time point and the waking time of participants was not reported Thus these results should be inter-
preted with caution (Woolery et al 2004)
325 Serum cortisol
Only one reviewed study collected serum cortisol Sarubin et al
found that1047297veweeks of hatha yoga alongsidewitheitheran SSRI or
an atypical antipsychotic did not in1047298uence daytime serum cortisol
levels when compared to the SSRI or an atypical antipsychotic
alone in individuals with major depressive disorder Since both
medications were seen to decrease cortisol levels over time it is
possible that the additive effects of yoga were too small to be
detected Additionally the authors noted that the yoga intervention
used in this trial (5 60 min over 1047297ve weeks) was arguably too
short to result in endocrinological changes (Sarubin et al 2014)
326 Autonomic measures
There is strong evidence for the bene1047297cial effects of yoga on
stress-related autonomic measures such as blood pressure and
heart rate One small study by Tolbanos Roche et al involving 20
individuals with hypertension showed that a yoga program was
associated with reduced blood pressure stress anxiety and nega-
tive affect (Tolbanos Roche and Mas Hesse 2014) In 238 individuals
with hypertension Sujatha et al demonstrated that a 12 week
hatha yoga program was associated with a decrease in heart rate
blood pressure anxiety and perceivedstress compared to a waitlist
control group (Sujatha and J A 2014) In healthy women Kanojia
et al demonstrated that yoga decreased premenstrual associated
increases in blood pressure anger depression and anxiety and was
associated with a lower heart rate when compared to a no treat-
ment control group This effect was statistically signi1047297cant in the
second and third menstrual cycle after beginning practice (Kanojia
et al 2013) Innes et al showed that an eight-week Iyenger yoga
program decreased blood pressure anxiety perceived stress and
improved mood and sleep quality in women with restless-leg
syndrome when compared to individuals exposed to an educa-
tional 1047297lm program (Innes and Selfe 2012) In a trial involving
patients with osteoarthritis of the knee Ebnezar et alreported that
yoga in conjunction with conventional physiotherapy was associ-
ated with reduced blood pressure heart rate anxiety pain and
stiffness compared to physiotherapy exercises alone (Ebnezar et al
2012) These results suggest that yoga practices may have mood
and nervous system mediating effects beyond those associated
with targeted physical rehabilitation McDermott et al found that
eight weeks of either yoga or walking decreased blood pressure
anxiety depression and perceived stress with no difference be-
tween intervention groups on these measures in people with
elevated blood glucose (McDermott et al 2014) Finally Malathi
et al showed that in a sample of 75 healthy university students
that three months of yoga or relaxation was associated with
decreased changes in heart rate blood pressure galvanic skin
relaxation and anxiety during examination period as compared toa no treatment control group (Malathi et al 1998)
Only two studies measured the in1047298uence of yoga practice on
HRV Cheema et al found no effect of yoga practice on HRV in
healthy individuals but instead found that yoga was associated
with increased resting heart rate At baseline the yoga group had a
lower resting heart rate than the control group representing a
possible sampling bias (yoga group 62 plusmn 6 beatsmin control group
68 plusmn 10 beatsmin) The authors stipulated that the post interven-
tion increase in heart rate might have represented regression to the
mean in the yoga group Indeed heart rate was seen to be similar
between groups post intervention (yoga group 65 plusmn 9 beatsmin
control group 67 plusmn 9 beatsmin) (Cheema et al 2013) Telles et al
similarly failed to demonstrate an increase in HRV among 1047298ood
survivors in the single study investigating Patanjali Yogacompared to a wait list control group Telles et al speculated that
this lack of difference between groups might have been due to the
short one-week intervention period or low statistical power ( Telles
et al 2010) Thus in these two studies it appears that yoga practice
does not increase parasympathetic nervous system activity or
improve the balance between the sympathetic and para-
sympathetic systems
327 Immune changes
In a trial involving 186 breast cancer survivors Kiecolt-Glaser
et al demonstrated that a hatha yoga program reduced the pro-
duction of Interleukin-6 Tumor Necrosis Factor-alpha and Inter-
lukin-1beta cytokine from isolated peripheral blood mononuclear
cells stimulated with lipopolysaccharide (the major component of the outer membrane of Gram-negative bacteria which is often used
to induce an acute immune response (Kulp and Kuehn 2010)) as
well as decreasedfatigue and increased vitality but hadno effecton
depression scores compared to a waitlist control group when
measured at three months follow up from the 12 week program
Yoga participants did not report changes in perceived social sup-
port compared to the control group suggesting that social support
was not a mediating factor in their 1047297ndings (Kiecolt-Glaser et al
2014) Gopal et al showed that in university students 12 weeks
of yoga before examinations was associated with less exam related
increases in serum cortisol and decreases in the cytokine Inter-
feron gamma (IFN-g) Decreased serum IFN-g indicates a decline in
cellular immunity and thus the authors interpreted these 1047297ndings
to suggest that yoga may protect against stress related immune
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suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 279
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more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Jorm AF et al 2000 Public belief systems about the helpfulness of interventionsfor depression associations with history of depression and professional help-seeking Soc Psychiatry Psychiatr Epidemiol 35 (5) 211e219
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Kinser PA Goehler LE Taylor AG 2012 How might yoga help depression a
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Kudielka BM Kirschbaum C 2003 Awakening cortisol responses are in1047298uencedby health status and awakening time but not by menstrual cycle phase Psy-choneuroendocrinology 28 (1) 35e47
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MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 281
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httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1313
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MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282282
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1013
suppression during situations of high stress (Gopal et al 2011)
Based on these 1047297ndings it appears that changes in cytokine levels
associated with yoga practice may contribute to changes in
behavioural outcomes
328 Yoga and brain measures
As illustrated in Table 1 only one RCT to date has collected both
measures of brain functioning in individuals practising yoga
(Streeter et al 2010b) Thestudy by Streeter et al was conducted in
the United States and included a cohort of mentally healthy in-
dividuals The authors used magnetic resonance spectroscopy
(MRS) prior to and following a 12-week Iyengar yoga or walking
program to determine Gamma-Aminobutyric Acid (GABA) levels in
the thalamic regions Notably this important neurotransmitter is
reduced across the spectrum of mood disorders This study
demonstrated that yoga was associated with decreased anxiety and
improved mood Further GABA levels positively correlated with
mood scores and negatively correlated with anxiety scores
(Streeter et al 2010b) The positive correlation between GABA
levels and mood scores suggests that GABA may at least in part
mediate the bene1047297ts of yoga on mood The link between the GABA
system and the in1047298ammatory response is still equivocal Current
models of allostatic stress in psychiatry state that exposure totrauma has negative physiological effects and may induce a
decrease in GABA levels which is an indicator of increased
in1047298ammation (McEwen 2003) Therefore it could be argued that
the reduction in GABA levels observed in the Streeter et al study
may be associated with stress and that yoga counteracts this pro-
cess by inhibiting the functioning of the HPA system (Streeter et al
2012)
We were unable to identify any further RCTs investigating the
effects of yoga practice on mood and functional connectivity We
did however identify two small pre-post intervention studies In
one such study from the United States and involving 4 yoga naive
individuals participants were seen to have a decreased resting
cerebral blood 1047298ow ratio in the right amygdala dorsal medial cor-
tex and sensorimotor area after 12 weeks of Iyanger yogacompared to baseline and assessed using single-photon emission
computed tomography Additionally the change in cerebral blood
1047298ow from baseline to after a mediation session was smaller in the
dorsal medial frontal lobe PFC and right sensorimotor cortex post
12 weeks of Iyanger yoga compared to at baseline ( Cohen et al
2009) In another small pre-post intervention study from India
and involving seven healthy elderly individuals six months of yoga
practice comprising of asanas and pranayama was reported to in-
crease hippocampal volume as assessed using magnetic resonance
imaging (Hariprasad et al 2013) Neither of the two above dis-
cussed pre-post intervention studies had a mood or well-being
related outcome measure
33 Differences in yoga forms and studied populations on arousal
The reviewed studies varied greatly in terms of the studied
populations forms of yoga practiced and biological outcomes In
terms of trials using a hatha yoga based intervention one study by
Sujatha et al showed that yoga was associated with changes in
blood pressure and heart rate (Sujatha and J A 2014) Smith et al
found no effect of hatha yoga practice on blood pressure (Smith
et al 2007) and Cheema et al found no effect of hatha yoga
practice on HRV (Cheema et al 2013) The studies by Smith et al
and Cheema et al only required participant to engage in 150 min
and 60 min of yoga practice a week respectively (Smith et al 2007
Cheema et al 2013) This was compared to compared to 600 min
followed by at least 150 min a week in the study by Sujatha et al
(Sujatha and J A 2014) One hatha yoga based study by Danucalov
et al showed a change in salivary cortisol (Danucalov et al 2013)
while a second hatha yoga study by Sarubin et al reported no
change in serum cortisol (Sarubin et al 2014) The Sarubin et al
study only required participants to engage in 60 min of practice a
week for 1047297ve weeks (Sarubin et al 2014) compared to 225 min a
week for eight weeks in the study by Danucalov et al (Danucalov
et al 2013) Kiecolt-Glaser et al (Kiecolt-Glaser et al 2014)
found that in 186 breast cancer survivors that women who prac-
ticed hatha yoga for a longer time period each day showed greater
reductions in fatigue and increases in vitality at post treatment and
three months follow up as well as a greater decease in lipopoly-
saccharide stimulated Interleukin-6 and Interlukin-1beta produc-
tion from isolated peripheral blood mononuclear cell at three
months follow up from the 12 week program As little as a 10 min
increase in daily yoga practice was associated with a 1047297ve-
percentage decrease in the IL-6 and an eight-percentage decrease
IL-1b geometric mean (Kiecolt-Glaser et al 2014) Thus collectively
these studies suggest that the dose of yoga practice is likely an
important mediating factor in terms of modulation of the SNS or
levels of the stress hormone cortisol
A further possible mediating factor on the effect of yoga on
biological outcomes is the population studied In the three hatha
yoga studies that found no biological changes the included patientswere those with major depressive disorder or healthy adults (Smith
et al 2007 Cheema et al 2013 Sarubin et al 2014) In the three
hatha yoga studies that reported a biological effect the participants
were breast cancer survivors individuals with hypertension and
healthy familial caregivers (Sujatha and J A 2014 Kiecolt-Glaser
et al 2014 Danucalov et al 2013) It is therefore possible that
yoga practice mediates SNS activation more effectively in some
populations than in others For example prenatal yoga was seen to
decrease salivary cortisol in both of the reviewed studies involving
pregnant women (Field et al 2013 Newham et al 2014) even
when only practiced for 20 min a week for 12 weeks ( Field et al
2013) Cortisol endogenously elevates during pregnancy and thus
this population mayshow a greater likelihood of decreasing cortisol
(Mastorakos and Ilias 2003) It is also possible that the effects of theyoga practice are great enough to elicit a decrease in cortisol in
spite of elevated levels
Biological outcomes were available for only three studies
investigating the effects of Iyengar yoga two of which involved
healthy adults and found no effect on salivary cortisol (Woolery
et al 2004 Bowden et al 2012) One study involved women
with restless leg syndrome and found that Iyengar yoga decreased
blood pressure but not heart rate (Innes and Selfe 2012) Restor-
ative yoga was similarly seen not to in1047298uence salivary cortisol in
one study (Corey et al 2014) Thus the preliminary data suggests
that hatha and prenatal yoga may be more effective than restor-
ative or Iyengar yoga in mediating SNS activity and the HPA axis It
is possible that Iyengar yoga does not effectively mediate SNS ac-
tivity in healthy individuals However there are too few studiesavailable and 1047297ndings are too inconsistent to draw conclusions in
this regard
Ten studies did not specify the type of yoga interventions used
however 1047297ve of these were seen to in1047298uence heart rate andor
blood pressure (McDermott et al 2014 Kanojia et al 2013
Ebnezar et al 2012 Malathi et al 1998 Tolbanos Roche and Mas
Hesse 2014) two were seen to in1047298uence salivary cortisol
(Vadiraja et al 2009 Chandwani et al 2014) and one to in1047298uence
serum cortisol and IFN-g but not heart rate or blood pressure
(Gopal et al 2011)
Overall the studies reviewed provide preliminary evidence that
various forms of yoga practice including hatha and prenatal yoga
are associated with biological changes including cortisol levels SNS
activation decreased stress and negative affect Programs involving
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 279
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1113
more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Ding D Stamatakis E 2014 Yoga practice in England 1997e2008 prevalencetemporal trends and correlates of participation BMC Res Notes 7 172
Drevets WC1998 Functional neuroimaging studies of depression the anatomy of melancholia Annu Rev Med 49 341e361
Drevets WC 1999 Prefrontal cortical-amygdalar metabolism in major depressionAdv Ventral Striatum Ext Amygdala 877 614e637
Ebnezar J et al 2012 Effect of integrated yoga therapy on pain morning stiffness
and anxiety in osteoarthritis of the knee joint a randomized control study Int J Yoga 5 (1) 28e36Edwards S et al 2001 Exploration of the awakening cortisol response in relation
to diurnal cortisol secretory activity Life Sci 68 (18) 2093e2103Eison MS 1990 Serotonin a common neurobiologic substrate in anxiety and
depression J Clin Psychopharmacol 10 (3 Suppl l) 26Se30SEren I et al 2003 Evaluation of regional cerebral blood 1047298ow changes in panic
disorder with Tc99m-HMPAO SPECT Psychiatry Research-Neuroimaging 123(2) 135e143
Farmer J 2012 Yoga body the origins of modern posture practice Rev Am Hist40 (1) 145e158
Field T et al 2013 Yoga and social support reduce prenatal depression anxietyand cortisol J Bodyw Mov Ther 17 (4) 397e403
Fries GR et al 2012 Staging and neuroprogression in bipolar disorder CurrPsychiatry Rep 14 (6) 667e675
Frodl T et al 2002 Hippocampal changes in patients with a 1047297rst episode of majordepression Am J Psychiatry 159 (7) 1112e1118
G F 1998 The Yoga Tradition Hohm Press PrescottGaykema RP Goehler LE 2011 Ascending caudal medullary catecholamine
pathways drive sickness-induced de1047297cits in exploratory behavior brain sub-strates for fatigue Brain Behav Immun 25 (3) 443e460
Goehler LE et al 2000 Vagal immune-to-brain communication a visceral che-mosensory pathway Auton Neurosci 85 (1e3) 49e59
Goodyer IM et al 1996 Adrenal secretion during major depression in 8- to 16-year-olds 1 Altered diurnal rhythms in salivary cortisol and dehydroepian-drosterone (DHEA) at presentation Psychol Med 26 (2) 245e256
Gopal A et al 2011 Effect of integrated yoga practices on immune responses inexamination stress e a preliminary study Int J Yoga 4 (1) 26e32
Goyal M et al 2014 Meditation programs for psychological stress and well-beinga systematic review and meta-analysis JAMA Intern Med 174 (3) 357e368
Granath J et al 2006 Stress management a randomized study of cognitivebehavioural therapy and yoga Cogn Behav Ther 35 (1) 3e10
Granger DA et al 2009 Medication effects on salivary cortisol tactics andstrategy to minimize impact in behavioral and developmental science Psy-choneuroendocrinology 34 (10) 1437e1448
Gustavsson A et al 2011 Cost of disorders of the brain in Europe 2010 EurNeuropsychopharmacol 21 (10) 718e779
Hallgren M et al 2014 Yoga as an adjunct treatment for alcohol dependence apilot study Complement Ther Med 22 (3) 441e445
Harinath K et al 2004 Effects of Hatha yoga and Omkar meditation on cardio-respiratory performance psychologic pro1047297le and melatonin secretion J AlternComplement Med 10 (2) 261e268
Hariprasad VR et al 2013 Yoga increases the volume of the hippocampus inelderly subjects Indian J Psychiatry 55 (Suppl 3) S394eS396
Herman JP et al 2005 Limbic system mechanisms of stress regulationhypothalamo-pituitary-adrenocortical axis Prog Neuropsychopharmacol BiolPsychiatry 29 (8) 1201e1213
Howland RH 2006 Pharmacotherapy strategies for treatment-resistant depres-sion J Psychosoc Nurs Ment Health Serv 44 (11) 11e14
Hranov LG 2007 Comorbid anxiety and depression illumination of a controversyInt J Psychiatry Clin Pract 11 (3) 171e189
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Ionescu DF et al 2013 Neurobiology of anxious depression a review DepressAnxiety 30 (4) 374e385
Issakidis C Andrews G 2002 Service utilisation for anxiety in an Australiancommunity sample Soc Psychiatry Psychiatr Epidemiol 37 (4) 153e163
Jackson PL et al 2006 Empathy examined through the neural mechanismsinvolved in imagining how I feel versus how you f eel pain Neuropsychologia 44(5) 752e761
John PJ et al 2007 Effectiveness of yoga therapy in the treatment of migrainewithout aura a randomized controlled trial Headache 47 (5) 654e661
Johnson J Weissman MM Klerman GL 1990 Panic disorder comorbidity andsuicide attempts Arch Gen Psychiatry 47 (9) 805e808
Jorm AF et al 2000 Public belief systems about the helpfulness of interventionsfor depression associations with history of depression and professional help-seeking Soc Psychiatry Psychiatr Epidemiol 35 (5) 211e219
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MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282282
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1113
more hours of yoga practice per week seem to be more effective
than those with fewer hours Based on current 1047297ndings yoga does
not appear to mediate SNS or HPA activity as effectively in healthy
individuals However it is still unknown what aspects of the yoga
intervention are effective for example previous research shows
bene1047297cial effects of exercise (Craft and Perna 2004) meditation
(Goyal et al 2014) and mindfulness (Piet and Hougaard 2011) all
of which yoga practice encompasses
4 Discussion
Yoga is commonly used as a form of stress management
(Penman et al 2012) with practicing individuals reporting a
preference for self-management over clinical intervention no side
effects and a perceived ef 1047297cacy of yoga greater than that of con-
ventional medication (Pilkington et al 2005 Issakidis and
Andrews 2002 Jorm et al 2000a Jorm et al 2000b) The posi-
tive public perception of yoga is demonstrated by its growing
popularity In the United States approximately 95 of the popu-
lation were practising yoga in 2012 compared to 61 in 2007
(Clarke et al 2015) In Australia approximately 35 of the popu-
lation was practicing yoga in 2010 compared to 29 in 2006
(Australian Sports Commission and tSRGS 2010) In England upto 128 of the population were practicing in 200608 compared to
046 in 199799 (Ding and Stamatakis 2014) Accordingly medical
providers such as general practitioners are more commonly rec-
ommending yoga as a treatment method to their patients In the
United States approximately 144 million people where prescribed
yoga by their doctor in 2011 (Nerurkar et al 2011) A recent
Australian survey reports that 121 of general practitioners in New
South Wales recommended yoga therapies to their patients A
many as 766 of practitioners referred their patients to a yoga
therapist at least a few times during the year while 125 of
practitioners referred patients at least once per week (Wardle et al
2014)
Some individuals may 1047297nd yoga practice more appealing than
pharmacological therapies as it allows participants to be activelyengaged in therapy and as yoga can be utilised at periods of high
anxietydepression which empowers the individual in self-
management Additionally yoga practice may not be perceived to
lsquoarti1047297ciallyrsquo affect biochemical processes in the manner that phar-
maceutical interventions may be
However and despite the growing popularity of yoga practice
its neurobiological effects arestill largely notunderstood While the
literature-reviewed in the present systematic review suggests that
yoga practice appears to improve positive affect and decrease
depressive and anxious symptomology in diverse populations
many of the reviewed studies are characterised by small sample
size no follow up and the yoga interventions are not well
described making study replication and interpretation dif 1047297cult
Additionally in a number of studies the method of salivary cortisolcollection is characterised by a lack of rigor Indeed Table 1 shows
that many of the reviewed studies are published in lower impact
journals which at times can be re1047298ected by the methodological
quality of the studies Yoga research is a developing 1047297eld with a
dif 1047297cult to de1047297ne taxonomy (Ospina et al 2007) and arguably with
a reputation for poor methodological rigour This perception within
the scienti1047297c community may limit the availability of research
funding and thus further impair the production of high quality
research trials
Despite methodological limitations the large majority of the
studies provide some evidence that yoga is associated with bio-
logical changes in blood pressure heart rate cortisol or cytokine
levels It is therefore plausible that yoga may affect mood via SNS
and HPA axis regulation Further studies are required in order to
con1047297rm the preliminary1047297ndings that yoga appears to in1047298uence the
stress response and to explore the effects of yoga on the neural
correlates in the context of mood changes
Disclosurecon1047298ict of interest
The authors declare no con1047298ict of interest
Contributors
Michaela Celeste Pascoe designed the protocol conducted the
systematic review and wrote the manuscript Isabelle E Bauer
contributed to design of the protocol the systematic review and
the writing of the manuscript All authors have approved the 1047297nal
article
Role of the funding source
The was no funding source for this research
Acknowledgements
The authors have no acknowledgments to declare
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Ding D Stamatakis E 2014 Yoga practice in England 1997e2008 prevalencetemporal trends and correlates of participation BMC Res Notes 7 172
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Drevets WC 1999 Prefrontal cortical-amygdalar metabolism in major depressionAdv Ventral Striatum Ext Amygdala 877 614e637
Ebnezar J et al 2012 Effect of integrated yoga therapy on pain morning stiffness
and anxiety in osteoarthritis of the knee joint a randomized control study Int J Yoga 5 (1) 28e36Edwards S et al 2001 Exploration of the awakening cortisol response in relation
to diurnal cortisol secretory activity Life Sci 68 (18) 2093e2103Eison MS 1990 Serotonin a common neurobiologic substrate in anxiety and
depression J Clin Psychopharmacol 10 (3 Suppl l) 26Se30SEren I et al 2003 Evaluation of regional cerebral blood 1047298ow changes in panic
disorder with Tc99m-HMPAO SPECT Psychiatry Research-Neuroimaging 123(2) 135e143
Farmer J 2012 Yoga body the origins of modern posture practice Rev Am Hist40 (1) 145e158
Field T et al 2013 Yoga and social support reduce prenatal depression anxietyand cortisol J Bodyw Mov Ther 17 (4) 397e403
Fries GR et al 2012 Staging and neuroprogression in bipolar disorder CurrPsychiatry Rep 14 (6) 667e675
Frodl T et al 2002 Hippocampal changes in patients with a 1047297rst episode of majordepression Am J Psychiatry 159 (7) 1112e1118
G F 1998 The Yoga Tradition Hohm Press PrescottGaykema RP Goehler LE 2011 Ascending caudal medullary catecholamine
pathways drive sickness-induced de1047297cits in exploratory behavior brain sub-strates for fatigue Brain Behav Immun 25 (3) 443e460
Goehler LE et al 2000 Vagal immune-to-brain communication a visceral che-mosensory pathway Auton Neurosci 85 (1e3) 49e59
Goodyer IM et al 1996 Adrenal secretion during major depression in 8- to 16-year-olds 1 Altered diurnal rhythms in salivary cortisol and dehydroepian-drosterone (DHEA) at presentation Psychol Med 26 (2) 245e256
Gopal A et al 2011 Effect of integrated yoga practices on immune responses inexamination stress e a preliminary study Int J Yoga 4 (1) 26e32
Goyal M et al 2014 Meditation programs for psychological stress and well-beinga systematic review and meta-analysis JAMA Intern Med 174 (3) 357e368
Granath J et al 2006 Stress management a randomized study of cognitivebehavioural therapy and yoga Cogn Behav Ther 35 (1) 3e10
Granger DA et al 2009 Medication effects on salivary cortisol tactics andstrategy to minimize impact in behavioral and developmental science Psy-choneuroendocrinology 34 (10) 1437e1448
Gustavsson A et al 2011 Cost of disorders of the brain in Europe 2010 EurNeuropsychopharmacol 21 (10) 718e779
Hallgren M et al 2014 Yoga as an adjunct treatment for alcohol dependence apilot study Complement Ther Med 22 (3) 441e445
Harinath K et al 2004 Effects of Hatha yoga and Omkar meditation on cardio-respiratory performance psychologic pro1047297le and melatonin secretion J AlternComplement Med 10 (2) 261e268
Hariprasad VR et al 2013 Yoga increases the volume of the hippocampus inelderly subjects Indian J Psychiatry 55 (Suppl 3) S394eS396
Herman JP et al 2005 Limbic system mechanisms of stress regulationhypothalamo-pituitary-adrenocortical axis Prog Neuropsychopharmacol BiolPsychiatry 29 (8) 1201e1213
Howland RH 2006 Pharmacotherapy strategies for treatment-resistant depres-sion J Psychosoc Nurs Ment Health Serv 44 (11) 11e14
Hranov LG 2007 Comorbid anxiety and depression illumination of a controversyInt J Psychiatry Clin Pract 11 (3) 171e189
Innes KE Selfe TK 2012 The effects of a gentle yoga program on sleep moodand blood pressure in older women with restless legs syndrome (RLS) a pre-liminary randomized controlled trial Evid Based Complement Altern Med2012 294058
Ionescu DF et al 2013 Neurobiology of anxious depression a review DepressAnxiety 30 (4) 374e385
Issakidis C Andrews G 2002 Service utilisation for anxiety in an Australiancommunity sample Soc Psychiatry Psychiatr Epidemiol 37 (4) 153e163
Jackson PL et al 2006 Empathy examined through the neural mechanismsinvolved in imagining how I feel versus how you f eel pain Neuropsychologia 44(5) 752e761
John PJ et al 2007 Effectiveness of yoga therapy in the treatment of migrainewithout aura a randomized controlled trial Headache 47 (5) 654e661
Johnson J Weissman MM Klerman GL 1990 Panic disorder comorbidity andsuicide attempts Arch Gen Psychiatry 47 (9) 805e808
Jorm AF et al 2000 Public belief systems about the helpfulness of interventionsfor depression associations with history of depression and professional help-seeking Soc Psychiatry Psychiatr Epidemiol 35 (5) 211e219
Jorm AF et al 2000 Public beliefs about the helpfulness of interventions fordepression effects on actions taken when experiencing anxiety and depressionsymptoms Aust N Z J Psychiatry 34 (4) 619e626
Kanojia S et al 2013 Effect of yoga on autonomic functions and psychologicalstatus during both phases of menstrual cycle in young healthy females J ClinDiagn Res 7 (10) 2133e2139
Kempton MJ et al 2011 Structural neuroimaging studies in major depressivedisorder Meta-analysis and comparison with bipolar disorder Arch Gen Psy-chiatry 68 (7) 675e690
Kiecolt-Glaser JK et al 2014 Yogas impact on in1047298ammation mood and fatigue inbreast cancer survivors a randomized controlled trial J Clin Oncol 32 (10)1040e1049
King SL Hegadoren KM 2002 Stress hormones how do they measure up BiolRes Nurs 4 (2) 92e103
Kinser PA Goehler LE Taylor AG 2012 How might yoga help depression a
neurobiological perspective Explore J Sci Heal 8 (2) 118e
126Kirsch I et al 2008 Initial severity and antidepressant bene1047297ts a meta-analysis of data submitted to the food and drug Administration PLoS Med 5 (2) e45
Kjellgren A et al 2007 Wellness through a comprehensive yogic breathing pro-gram e a controlled pilot trial BMC Complement Altern Med 7 43
Krishnan V Nestler EJ 2008 The molecular neurobiology of depression Nature455 (7215) 894e902
Kubera M et al 2000 The effect of repeated amitriptyline and desipramineadministration on cytokine release in C57BL6 mice Psychoneuroendocrinology25 (8) 785e797
Kudielka BM Kirschbaum C 2003 Awakening cortisol responses are in1047298uencedby health status and awakening time but not by menstrual cycle phase Psy-choneuroendocrinology 28 (1) 35e47
Kulp A Kuehn MJ 2010 Biological functions and biogenesis of secreted bacterialouter membrane vesicles Annu Rev Microbiol 64 163e184
Li AW Goldsmith CA 2012 The effects of yoga on anxiety and stress AlternMed Rev 17 (1) 21e35
Lutz A DJ Davidson RJ 2007 Meditation and the neuroscience of consciousnessIn Z P (Ed) Cambridge Handbook of Consciousness Cambridge University
Press Cambridge pp 499e
554Maes M 2008a The cytokine hypothesis of depression in1047298ammation oxidative amp
nitrosative stress (IOampNS) and leaky gut as new targets for adjunctive treat-ments in depression Neuroendocrinol Lett 29 (3) 287e291
Maes M 2008b The cytokine hypothesis of depression in1047298ammation oxidative ampnitrosative stress (IOampNS) and leaky gut as new targets for adjunctive treat-ments in depression Neuro Endocrinol Lett 29 (3) 287e291
Malathi A et al 1998 Psychophysiological changes at the time of examination inmedical students before and after the practice of yoga and relaxation Indian JPsychiatry 40 (1) 35e40
Masi G Brovedani P 2011 The hippocampus neurotrophic factors and depres-sion possible implications for the pharmacotherapy of depression CNS Drugs25 (11) 913e931
Mastorakos G Ilias I 2003 Maternal and fetal hypothalamic-pituitary-adrenalaxes during pregnancy and postpartum Ann N Y Acad Sci 997 136e149
Mathew AR et al 2011 Co-morbidity between major depressive disorder andanxiety disorders shared etiology or direct causation Psychol Med 41 (10)2023e2034
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 281
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1313
McCall MC 2013 How might yoga work an overview of potential underlyingmechanisms Yoga Phys Ther 3 (1)
McDermott KA et al 2014 A yoga intervention for type 2 diabetes risk reductiona pilot randomized controlled trial BMC Complement Altern Med 14 212
McEwen BS 2003 Mood disorders and allostatic load Biol Psychiatry 54 (3)200e207
McIntyre RS et al 2010 The association between conventional antidepressantsand the metabolic syndrome a review of the evidence and clinical implicationsCns Drugs 24 (9) 741e753
Michel TM Pulschen D Thome J 2012 The role of oxidative stress in depressive
disorders Curr Pharm Des 18 (36) 5890e
5899Miller EK Freedman DJ Wallis JD 2002 The prefrontal cortex categories
concepts and cognition Philos Trans R Soc Lond B Biol Sci 357 (1424)1123e1136
Morilak DA Frazer A 2004 Antidepressants and brain monoaminergic systemsa dimensional approach to understanding their behavioural effects in depres-sion and anxiety disorders Int J Neuropsychopharmacol 7 (2) 193e218
Musselman DL et al 2001 Paroxetine for the prevention of depression inducedby high-dose interferon alfa N Engl J Med 344 (13) 961e966
Neale MC Kendler KS 1995 Models of comorbidity for multifactorial disordersAm J Hum Genet 57 (4) 935e953
Nerurkar A et al 2011 When conventional medical providers recommend un-conventional medicine results of a national study Arch Intern Med 171 (9)862e864
Newham JJ et al 2014 Effects of antenatal yoga on maternal anxiety anddepression a randomized controlled trial Depress Anxiety 31 (8) 631e640
Nutt D Argyropoulos S F S 1998 Generalized Anxiety Disorder DiagnosisTreatment and its Relationship to Other Anxiety Disorders Martin Dunitz Ltd London
Olesen J et al 2012 The economic cost of brain disorders in Europe Eur J Neurol19 (1) 155e162
Olson KL Marc DT Grude LA McManus CJ Kellermann GH 2012 Thehypothalamic-pituitary-adrenal axis the actions of the Central Nervous Systemand Potential Biomarkers In Klatz R Goldman R (Eds) Anti-aging Thera-peutics vol XIII American Academy of Anti-Aging Medicine Chicago IL USApp 91e100 201
Organisation WH 2013 Depression FactsheetOspina MB et al 2007 Meditation practices for health state of the research Evid
Rep Technol Assess (Full Rep) (155) 1e263Pascoe MC et al 2011 In1047298ammation and depression why poststroke depression
may be the norm and not the exception Int J Stroke 6 (2) 128e135Penman S et al 2012 Yoga in Australia results of a national survey Int J Yoga 5
(2) 92e101P1047298ueger LW 2011 Yoga body the origins of modern posture practice Relig Stud
Rev 37 (3) 235e235Piet J Hougaard E 2011 The effect of mindfulness-based cognitive therapy for
prevention of relapse in recurrent major depressive disorder a systematic re-
view and meta-analysis Clin Psychol Rev 31 (6) 1032e
1040Pilkington K et al 2005 Yoga for depression the research evidence J AffectDisord 89 (1e3) 13e24
Poll EM et al 2007 Saliva collection method affects predictability of serumcortisol Clin Chim Acta 382 (1e2) 15e19
Raison CL et al 2013 A randomized controlled trial of the tumor necrosis factorantagonist in1047298iximab for treatment-resistant depression the role of baselinein1047298ammatory biomarkers JAMA Psychiatry 70 (1) 31e41
Raison CL Capuron L Miller AH 2006 Cytokines sing the blues in1047298ammationand the pathogenesis of depression Trends Immunol 27 (1) 24e31
Rocha KK et al 2012 Improvement in physiological and psychological parame-ters after 6 months of yoga practice Conscious Cogn 21 (2) 843e850
Roy-Byrne PP et al 1986 The corticotropin-releasing hormone stimulation test inpatients with panic disorder Am J Psychiatry 143 (7) 896e899
Sapolsky RM Romero LM Munck AU 2000 How do glucocorticoids in1047298uencestress responses Integrating permissive suppressive stimulatory and pre-parative actions Endocr Rev 21 (1) 55e89
Sarubin N et al 2014 The in1047298uence of Hatha yoga as an add-on treatment inmajor depression on hypothalamic-pituitary-adrenal-axis activity a random-
ized trial J Psychiatr Res 53 76e
83Schatzberg AF 2007 Safety and tolerability of antidepressants weighing the
impact on treatment decisions J Clin Psychiatry 68 (Suppl 8) 26e34Schulberg HC Katon WJ S MK 1998 Management of mood and anxiety dis-
orders in primary care In Rush AJ (Ed) Mood and Anxiety Disorders CurrentScience Inc Philadelphia PA
Sharma VK et al 2006 Effect of Sahaj Yoga on neuro-cognitive functions in pa-tients suffering from major depression Indian J Physiol Pharmacol 50 (4)375e383
Sheline YI Gado MH Kraemer HC 2003 Untreated depression and hippo-campal volume loss Am J Psychiatry 160 (8) 1516e1518
Shyn SI Hamilton SP 2010 The genetics of major depression moving beyondthe monoamine hypothesis Psychiatr Clin North Am 33 (1) 125e140
Siegle GJ et al 2002 Cant shake that feeling assessment of sustained event-related fMRI amygdala activity in response to emotional information indepressed individuals Biol Psychiatry 51 (9) 693e707
da Silva TL Ravindran LN Ravindran AV 2009 Yoga in the treatment of moodand anxiety disorders a review Asian J Psychiatr 2 (1) 6e16
Silverman MN Sternberg EM 2012 Glucocorticoid regulation of in1047298ammationand its functional correlates from HPA axis to glucocorticoid receptordysfunction Ann N Y Acad Sci 1261 55e63
Smith C et al 2007 A randomised comparative trial of yoga and relaxation toreduce stress and anxiety Complement Ther Med 15 (2) 77e83
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern Complement Med16 (11) 1145e1152
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern ComplementaryMed 16 (11) 1145e1152
Streeter CC et al 2012 Effects of yoga on the autonomic nervous system gamma-aminobutyric-acid and allostasis in epilepsy depression and post-traumaticstress disorder Med Hypotheses 78 (5) 571e579
Sujatha T J A 2014 Efectivenes of a 12-Wek yoga program on physiopsychologicalparameters in patients with hypertension Int J Pharm Clin Res 6 (4)329e335
Telles S et al 2010 Post traumatic stress symptoms and heart rate variability inBihar 1047298ood survivors following yoga a randomized controlled study BMCPsychiatry 10 18
Tindle HA et al 2005 Trends in use of complementary and alternative medicineby us adults 1997-2002 Altern Ther Health Med 11 (1) 42e49
Tolbanos Roche L Mas Hesse B 2014 Application of an integrative yoga therapyprogramme in cases of essential arterial hypertension in public healthcareComplement Ther Clin Pract 20 (4) 285e290 httpdxdoiorg101016
jctcp201410004Travis F Pearson C 200 0 Pure consciousness distinct phenomenological and
physiological correlates of ldquoconsciousness itself rdquo Int J Neurosci 100 (1e4)77e89
Uebelacker LA et al 2010 Hatha yoga for depression critical review of the evi-dence for ef 1047297cacy plausible mechanisms of action and directions for futureresearch J Psychiatr Pract 16 (1) 22e33
Vadiraja HS et al 2009 Effects of a yoga program on cortisol rhythm and moodstates in early breast cancer patients undergoing adjuvant radiotherapy arandomized controlled trial Integr Cancer Ther 8 (1) 37e46
Wardle J Adams J Sibbritt D 2014 Referral to yoga therapists in rural primaryhealth care a survey of general practitioners in rural and regional New SouthWales Australia Int J Yoga 7 (1) 9e16
Weibel L 2003 Methodological guidelines for the use of salivary cortisol as bio-logical marker of stress Presse Med 32 (18) 845e851
West J et al 2004 Effects of Hatha yoga and African dance on perceived stressaffect and salivary cortisol Ann Behav Med 28 (2) 114e118
Whiteford HA et al 2013 Global burden of disease attributable to mental andsubstance use disorders 1047297ndings from the global Burden of Disease Study 2010Lancet 382 (9904) 1575e1586
Wittchen HU et al 2011 The size and burden of mental disorders and otherdisorders of the brain in Europe 2010 Eur Neuropsychopharmacol 21 (9)655e679
Woolery A et al 2004 A yoga intervention for young adults with elevatedsymptoms of depression Altern Ther Health Med 10 (2) 60e63
Yang Y Raine A 2009 Prefrontal structural and functional brain imaging 1047297ndingsin antisocial violent and psychopathic individuals a meta-analysis PsychiatryRes 174 (2) 81e88
Yeung A et al 2014 Randomised controlled trial of a 12 week yoga intervention
on negative affective states cardiovascular and cognitive function in post-cardiac rehabilitation patients BMC Complement Altern Med 14 411
del Zoppo G et al 2000 In1047298ammation and stroke putative role for cytokinesadhesion molecules and iNOS in brain response to ischemia Brain Pathol10 (1)95e112
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282282
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1213
Chattha R et al 2008 Treating the climacteric symptoms in Indian women withan integrated approach to yoga therapy a randomized control study Meno-pause 15 (5) 862e870
Cheema BS et al 2013 Effect of an of 1047297ce worksite-based yoga program on heartrate variability outcomes of a randomized controlled trial BMC ComplementAltern Med 13 82
Chen KW et al 2012 Meditative therapies for reducing anxiety a systematicreview and meta-analysis of randomized controlled trials Depress Anxiety 29(7) 545e562
Clarke TC et al 2015 Trends in the use of complementary health approaches
among adults United States 2002e
2012 Natl Health Stat Rep (79) 1e
16Clow A et al 2004 The awakening cortisol response methodological issues and
signi1047297cance Stress 7 (1) 29e37Cohen DL et al 2009 Cerebral blood 1047298ow effects of yoga training preliminary
evaluation of 4 cases J Altern Complement Med 15 (1) 9e14Corey SM et al 2014 Effect of restorative yoga vs stretching on diurnal cortisol
dynamics and psychosocial outcomes in individuals with the metabolic syn-drome the PRYSMS randomized controlled trial Psychoneuroendocrinology49 260e271
Craft LL Perna FM 2004 The bene1047297ts of exercise for the clinically depressedPrim Care Companion J Clin Psychiatry 6 (3) 104e111
Craig AD 2003 Interoception the sense of the physiological condition of thebody Curr Opin Neurobiol 13 (4) 500e505
Cramer H et al 2013 Yoga for depression a systematic review and meta-analysisDepress Anxiety 30 (11) 1068e1083
DSilva S et al 2012 Mind-body medicine therapies for a range of depressionseverity a systematic review Psychosomatics 53 (5) 407e423
Dantzer R 2012 Depression and in1047298ammation an intricate relationship BiolPsychiatry 71 (1) 4e5
Dantzer R et al 2008 From in1047298ammation to sickness and depression when theimmune system subjugates the brain Nat Rev Neurosci 9 (1) 46e56
Danucalov MA et al 2013 A yoga and compassion meditation program reducesstress in familial caregivers of Alzheimers disease patients Evid Based Com-plement Altern Med 2013 513149
Davidson RJ 2003 Affective neuroscience and psychophysiology toward a syn-thesis Psychophysiology 40 (5) 655e665
Davis M 1992 The role of the amygdala in fear and anxiety Annu Rev Neurosci15 353e375
Decety J Jackson PL 2004 The functional architecture of human empathy BehavCogn Neurosci Rev 3 (2) 71e100
Ding D Stamatakis E 2014 Yoga practice in England 1997e2008 prevalencetemporal trends and correlates of participation BMC Res Notes 7 172
Drevets WC1998 Functional neuroimaging studies of depression the anatomy of melancholia Annu Rev Med 49 341e361
Drevets WC 1999 Prefrontal cortical-amygdalar metabolism in major depressionAdv Ventral Striatum Ext Amygdala 877 614e637
Ebnezar J et al 2012 Effect of integrated yoga therapy on pain morning stiffness
and anxiety in osteoarthritis of the knee joint a randomized control study Int J Yoga 5 (1) 28e36Edwards S et al 2001 Exploration of the awakening cortisol response in relation
to diurnal cortisol secretory activity Life Sci 68 (18) 2093e2103Eison MS 1990 Serotonin a common neurobiologic substrate in anxiety and
depression J Clin Psychopharmacol 10 (3 Suppl l) 26Se30SEren I et al 2003 Evaluation of regional cerebral blood 1047298ow changes in panic
disorder with Tc99m-HMPAO SPECT Psychiatry Research-Neuroimaging 123(2) 135e143
Farmer J 2012 Yoga body the origins of modern posture practice Rev Am Hist40 (1) 145e158
Field T et al 2013 Yoga and social support reduce prenatal depression anxietyand cortisol J Bodyw Mov Ther 17 (4) 397e403
Fries GR et al 2012 Staging and neuroprogression in bipolar disorder CurrPsychiatry Rep 14 (6) 667e675
Frodl T et al 2002 Hippocampal changes in patients with a 1047297rst episode of majordepression Am J Psychiatry 159 (7) 1112e1118
G F 1998 The Yoga Tradition Hohm Press PrescottGaykema RP Goehler LE 2011 Ascending caudal medullary catecholamine
pathways drive sickness-induced de1047297cits in exploratory behavior brain sub-strates for fatigue Brain Behav Immun 25 (3) 443e460
Goehler LE et al 2000 Vagal immune-to-brain communication a visceral che-mosensory pathway Auton Neurosci 85 (1e3) 49e59
Goodyer IM et al 1996 Adrenal secretion during major depression in 8- to 16-year-olds 1 Altered diurnal rhythms in salivary cortisol and dehydroepian-drosterone (DHEA) at presentation Psychol Med 26 (2) 245e256
Gopal A et al 2011 Effect of integrated yoga practices on immune responses inexamination stress e a preliminary study Int J Yoga 4 (1) 26e32
Goyal M et al 2014 Meditation programs for psychological stress and well-beinga systematic review and meta-analysis JAMA Intern Med 174 (3) 357e368
Granath J et al 2006 Stress management a randomized study of cognitivebehavioural therapy and yoga Cogn Behav Ther 35 (1) 3e10
Granger DA et al 2009 Medication effects on salivary cortisol tactics andstrategy to minimize impact in behavioral and developmental science Psy-choneuroendocrinology 34 (10) 1437e1448
Gustavsson A et al 2011 Cost of disorders of the brain in Europe 2010 EurNeuropsychopharmacol 21 (10) 718e779
Hallgren M et al 2014 Yoga as an adjunct treatment for alcohol dependence apilot study Complement Ther Med 22 (3) 441e445
Harinath K et al 2004 Effects of Hatha yoga and Omkar meditation on cardio-respiratory performance psychologic pro1047297le and melatonin secretion J AlternComplement Med 10 (2) 261e268
Hariprasad VR et al 2013 Yoga increases the volume of the hippocampus inelderly subjects Indian J Psychiatry 55 (Suppl 3) S394eS396
Herman JP et al 2005 Limbic system mechanisms of stress regulationhypothalamo-pituitary-adrenocortical axis Prog Neuropsychopharmacol BiolPsychiatry 29 (8) 1201e1213
Howland RH 2006 Pharmacotherapy strategies for treatment-resistant depres-sion J Psychosoc Nurs Ment Health Serv 44 (11) 11e14
Hranov LG 2007 Comorbid anxiety and depression illumination of a controversyInt J Psychiatry Clin Pract 11 (3) 171e189
Innes KE Selfe TK 2012 The effects of a gentle yoga program on sleep moodand blood pressure in older women with restless legs syndrome (RLS) a pre-liminary randomized controlled trial Evid Based Complement Altern Med2012 294058
Ionescu DF et al 2013 Neurobiology of anxious depression a review DepressAnxiety 30 (4) 374e385
Issakidis C Andrews G 2002 Service utilisation for anxiety in an Australiancommunity sample Soc Psychiatry Psychiatr Epidemiol 37 (4) 153e163
Jackson PL et al 2006 Empathy examined through the neural mechanismsinvolved in imagining how I feel versus how you f eel pain Neuropsychologia 44(5) 752e761
John PJ et al 2007 Effectiveness of yoga therapy in the treatment of migrainewithout aura a randomized controlled trial Headache 47 (5) 654e661
Johnson J Weissman MM Klerman GL 1990 Panic disorder comorbidity andsuicide attempts Arch Gen Psychiatry 47 (9) 805e808
Jorm AF et al 2000 Public belief systems about the helpfulness of interventionsfor depression associations with history of depression and professional help-seeking Soc Psychiatry Psychiatr Epidemiol 35 (5) 211e219
Jorm AF et al 2000 Public beliefs about the helpfulness of interventions fordepression effects on actions taken when experiencing anxiety and depressionsymptoms Aust N Z J Psychiatry 34 (4) 619e626
Kanojia S et al 2013 Effect of yoga on autonomic functions and psychologicalstatus during both phases of menstrual cycle in young healthy females J ClinDiagn Res 7 (10) 2133e2139
Kempton MJ et al 2011 Structural neuroimaging studies in major depressivedisorder Meta-analysis and comparison with bipolar disorder Arch Gen Psy-chiatry 68 (7) 675e690
Kiecolt-Glaser JK et al 2014 Yogas impact on in1047298ammation mood and fatigue inbreast cancer survivors a randomized controlled trial J Clin Oncol 32 (10)1040e1049
King SL Hegadoren KM 2002 Stress hormones how do they measure up BiolRes Nurs 4 (2) 92e103
Kinser PA Goehler LE Taylor AG 2012 How might yoga help depression a
neurobiological perspective Explore J Sci Heal 8 (2) 118e
126Kirsch I et al 2008 Initial severity and antidepressant bene1047297ts a meta-analysis of data submitted to the food and drug Administration PLoS Med 5 (2) e45
Kjellgren A et al 2007 Wellness through a comprehensive yogic breathing pro-gram e a controlled pilot trial BMC Complement Altern Med 7 43
Krishnan V Nestler EJ 2008 The molecular neurobiology of depression Nature455 (7215) 894e902
Kubera M et al 2000 The effect of repeated amitriptyline and desipramineadministration on cytokine release in C57BL6 mice Psychoneuroendocrinology25 (8) 785e797
Kudielka BM Kirschbaum C 2003 Awakening cortisol responses are in1047298uencedby health status and awakening time but not by menstrual cycle phase Psy-choneuroendocrinology 28 (1) 35e47
Kulp A Kuehn MJ 2010 Biological functions and biogenesis of secreted bacterialouter membrane vesicles Annu Rev Microbiol 64 163e184
Li AW Goldsmith CA 2012 The effects of yoga on anxiety and stress AlternMed Rev 17 (1) 21e35
Lutz A DJ Davidson RJ 2007 Meditation and the neuroscience of consciousnessIn Z P (Ed) Cambridge Handbook of Consciousness Cambridge University
Press Cambridge pp 499e
554Maes M 2008a The cytokine hypothesis of depression in1047298ammation oxidative amp
nitrosative stress (IOampNS) and leaky gut as new targets for adjunctive treat-ments in depression Neuroendocrinol Lett 29 (3) 287e291
Maes M 2008b The cytokine hypothesis of depression in1047298ammation oxidative ampnitrosative stress (IOampNS) and leaky gut as new targets for adjunctive treat-ments in depression Neuro Endocrinol Lett 29 (3) 287e291
Malathi A et al 1998 Psychophysiological changes at the time of examination inmedical students before and after the practice of yoga and relaxation Indian JPsychiatry 40 (1) 35e40
Masi G Brovedani P 2011 The hippocampus neurotrophic factors and depres-sion possible implications for the pharmacotherapy of depression CNS Drugs25 (11) 913e931
Mastorakos G Ilias I 2003 Maternal and fetal hypothalamic-pituitary-adrenalaxes during pregnancy and postpartum Ann N Y Acad Sci 997 136e149
Mathew AR et al 2011 Co-morbidity between major depressive disorder andanxiety disorders shared etiology or direct causation Psychol Med 41 (10)2023e2034
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282 281
7262019 documento cientifico de la Yogapdf
httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 1313
McCall MC 2013 How might yoga work an overview of potential underlyingmechanisms Yoga Phys Ther 3 (1)
McDermott KA et al 2014 A yoga intervention for type 2 diabetes risk reductiona pilot randomized controlled trial BMC Complement Altern Med 14 212
McEwen BS 2003 Mood disorders and allostatic load Biol Psychiatry 54 (3)200e207
McIntyre RS et al 2010 The association between conventional antidepressantsand the metabolic syndrome a review of the evidence and clinical implicationsCns Drugs 24 (9) 741e753
Michel TM Pulschen D Thome J 2012 The role of oxidative stress in depressive
disorders Curr Pharm Des 18 (36) 5890e
5899Miller EK Freedman DJ Wallis JD 2002 The prefrontal cortex categories
concepts and cognition Philos Trans R Soc Lond B Biol Sci 357 (1424)1123e1136
Morilak DA Frazer A 2004 Antidepressants and brain monoaminergic systemsa dimensional approach to understanding their behavioural effects in depres-sion and anxiety disorders Int J Neuropsychopharmacol 7 (2) 193e218
Musselman DL et al 2001 Paroxetine for the prevention of depression inducedby high-dose interferon alfa N Engl J Med 344 (13) 961e966
Neale MC Kendler KS 1995 Models of comorbidity for multifactorial disordersAm J Hum Genet 57 (4) 935e953
Nerurkar A et al 2011 When conventional medical providers recommend un-conventional medicine results of a national study Arch Intern Med 171 (9)862e864
Newham JJ et al 2014 Effects of antenatal yoga on maternal anxiety anddepression a randomized controlled trial Depress Anxiety 31 (8) 631e640
Nutt D Argyropoulos S F S 1998 Generalized Anxiety Disorder DiagnosisTreatment and its Relationship to Other Anxiety Disorders Martin Dunitz Ltd London
Olesen J et al 2012 The economic cost of brain disorders in Europe Eur J Neurol19 (1) 155e162
Olson KL Marc DT Grude LA McManus CJ Kellermann GH 2012 Thehypothalamic-pituitary-adrenal axis the actions of the Central Nervous Systemand Potential Biomarkers In Klatz R Goldman R (Eds) Anti-aging Thera-peutics vol XIII American Academy of Anti-Aging Medicine Chicago IL USApp 91e100 201
Organisation WH 2013 Depression FactsheetOspina MB et al 2007 Meditation practices for health state of the research Evid
Rep Technol Assess (Full Rep) (155) 1e263Pascoe MC et al 2011 In1047298ammation and depression why poststroke depression
may be the norm and not the exception Int J Stroke 6 (2) 128e135Penman S et al 2012 Yoga in Australia results of a national survey Int J Yoga 5
(2) 92e101P1047298ueger LW 2011 Yoga body the origins of modern posture practice Relig Stud
Rev 37 (3) 235e235Piet J Hougaard E 2011 The effect of mindfulness-based cognitive therapy for
prevention of relapse in recurrent major depressive disorder a systematic re-
view and meta-analysis Clin Psychol Rev 31 (6) 1032e
1040Pilkington K et al 2005 Yoga for depression the research evidence J AffectDisord 89 (1e3) 13e24
Poll EM et al 2007 Saliva collection method affects predictability of serumcortisol Clin Chim Acta 382 (1e2) 15e19
Raison CL et al 2013 A randomized controlled trial of the tumor necrosis factorantagonist in1047298iximab for treatment-resistant depression the role of baselinein1047298ammatory biomarkers JAMA Psychiatry 70 (1) 31e41
Raison CL Capuron L Miller AH 2006 Cytokines sing the blues in1047298ammationand the pathogenesis of depression Trends Immunol 27 (1) 24e31
Rocha KK et al 2012 Improvement in physiological and psychological parame-ters after 6 months of yoga practice Conscious Cogn 21 (2) 843e850
Roy-Byrne PP et al 1986 The corticotropin-releasing hormone stimulation test inpatients with panic disorder Am J Psychiatry 143 (7) 896e899
Sapolsky RM Romero LM Munck AU 2000 How do glucocorticoids in1047298uencestress responses Integrating permissive suppressive stimulatory and pre-parative actions Endocr Rev 21 (1) 55e89
Sarubin N et al 2014 The in1047298uence of Hatha yoga as an add-on treatment inmajor depression on hypothalamic-pituitary-adrenal-axis activity a random-
ized trial J Psychiatr Res 53 76e
83Schatzberg AF 2007 Safety and tolerability of antidepressants weighing the
impact on treatment decisions J Clin Psychiatry 68 (Suppl 8) 26e34Schulberg HC Katon WJ S MK 1998 Management of mood and anxiety dis-
orders in primary care In Rush AJ (Ed) Mood and Anxiety Disorders CurrentScience Inc Philadelphia PA
Sharma VK et al 2006 Effect of Sahaj Yoga on neuro-cognitive functions in pa-tients suffering from major depression Indian J Physiol Pharmacol 50 (4)375e383
Sheline YI Gado MH Kraemer HC 2003 Untreated depression and hippo-campal volume loss Am J Psychiatry 160 (8) 1516e1518
Shyn SI Hamilton SP 2010 The genetics of major depression moving beyondthe monoamine hypothesis Psychiatr Clin North Am 33 (1) 125e140
Siegle GJ et al 2002 Cant shake that feeling assessment of sustained event-related fMRI amygdala activity in response to emotional information indepressed individuals Biol Psychiatry 51 (9) 693e707
da Silva TL Ravindran LN Ravindran AV 2009 Yoga in the treatment of moodand anxiety disorders a review Asian J Psychiatr 2 (1) 6e16
Silverman MN Sternberg EM 2012 Glucocorticoid regulation of in1047298ammationand its functional correlates from HPA axis to glucocorticoid receptordysfunction Ann N Y Acad Sci 1261 55e63
Smith C et al 2007 A randomised comparative trial of yoga and relaxation toreduce stress and anxiety Complement Ther Med 15 (2) 77e83
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern Complement Med16 (11) 1145e1152
Streeter CC et al 2010 Effects of yoga versus walking on mood anxiety and brainGABA levels a randomized controlled MRS study J Altern ComplementaryMed 16 (11) 1145e1152
Streeter CC et al 2012 Effects of yoga on the autonomic nervous system gamma-aminobutyric-acid and allostasis in epilepsy depression and post-traumaticstress disorder Med Hypotheses 78 (5) 571e579
Sujatha T J A 2014 Efectivenes of a 12-Wek yoga program on physiopsychologicalparameters in patients with hypertension Int J Pharm Clin Res 6 (4)329e335
Telles S et al 2010 Post traumatic stress symptoms and heart rate variability inBihar 1047298ood survivors following yoga a randomized controlled study BMCPsychiatry 10 18
Tindle HA et al 2005 Trends in use of complementary and alternative medicineby us adults 1997-2002 Altern Ther Health Med 11 (1) 42e49
Tolbanos Roche L Mas Hesse B 2014 Application of an integrative yoga therapyprogramme in cases of essential arterial hypertension in public healthcareComplement Ther Clin Pract 20 (4) 285e290 httpdxdoiorg101016
jctcp201410004Travis F Pearson C 200 0 Pure consciousness distinct phenomenological and
physiological correlates of ldquoconsciousness itself rdquo Int J Neurosci 100 (1e4)77e89
Uebelacker LA et al 2010 Hatha yoga for depression critical review of the evi-dence for ef 1047297cacy plausible mechanisms of action and directions for futureresearch J Psychiatr Pract 16 (1) 22e33
Vadiraja HS et al 2009 Effects of a yoga program on cortisol rhythm and moodstates in early breast cancer patients undergoing adjuvant radiotherapy arandomized controlled trial Integr Cancer Ther 8 (1) 37e46
Wardle J Adams J Sibbritt D 2014 Referral to yoga therapists in rural primaryhealth care a survey of general practitioners in rural and regional New SouthWales Australia Int J Yoga 7 (1) 9e16
Weibel L 2003 Methodological guidelines for the use of salivary cortisol as bio-logical marker of stress Presse Med 32 (18) 845e851
West J et al 2004 Effects of Hatha yoga and African dance on perceived stressaffect and salivary cortisol Ann Behav Med 28 (2) 114e118
Whiteford HA et al 2013 Global burden of disease attributable to mental andsubstance use disorders 1047297ndings from the global Burden of Disease Study 2010Lancet 382 (9904) 1575e1586
Wittchen HU et al 2011 The size and burden of mental disorders and otherdisorders of the brain in Europe 2010 Eur Neuropsychopharmacol 21 (9)655e679
Woolery A et al 2004 A yoga intervention for young adults with elevatedsymptoms of depression Altern Ther Health Med 10 (2) 60e63
Yang Y Raine A 2009 Prefrontal structural and functional brain imaging 1047297ndingsin antisocial violent and psychopathic individuals a meta-analysis PsychiatryRes 174 (2) 81e88
Yeung A et al 2014 Randomised controlled trial of a 12 week yoga intervention
on negative affective states cardiovascular and cognitive function in post-cardiac rehabilitation patients BMC Complement Altern Med 14 411
del Zoppo G et al 2000 In1047298ammation and stroke putative role for cytokinesadhesion molecules and iNOS in brain response to ischemia Brain Pathol10 (1)95e112
MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282282
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