13
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, Sweden b 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 Inammation 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 benecial for all individuals. There is evidence that yoga has mood-enhancing properties possibly related to its inhibitory effects on physiological stress and inammation, 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 decre ase in depr essive and anxious symptoms in a range of populati ons. Further research is warranted to conrm these preliminary  ndings and facilitate implementation in clinical settings. © 2015 Elsevier Ltd. All rights reserved. 1. Introduction 1.1. Mood, stress and brain changes Unipolar depression and anxiety are the leading source of adult disabili ty world wide (Shyn and Hamilton, 2010; Whiteford et al., 2013). Appro ximately 350 milli on peo ple are est imat ed to suff er fro m depressio n (Wor ld Health Organisation [WHO], 201 3) and associated societal costs are  V92 billion in Europe alone (Wittchen et al., 2011; Gustavsson et al., 2011; Olesen et al., 2012). Depression and anxiety are highly co-morbid with each other and have shared aetiolo gy and neur obiology (Neale and Ke ndler , 1995). Anxiet y is the single strongest predictor of depression onset ( Mathew et al., 2011; Avenevoli et al., 2001; Hranov, 2007). While there are neurochem- ical di fferences between the conditi ons, recent st udies vie w depr ession and anxiety as over lapping syndromes, existing on a continuum (Hranov, 2007; Bal dwi n et al., 2002; Ionesc u et al., 201 3). Depr ession and anxiety are clos ely linked to structur al 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 pers onalit y trait s (Mil ler et al. , 2002; Yang and Rai ne, 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  rst-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 ri sk fac tor 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: michaela.pasco [email protected] (M.C. Pascoe). Contents lists available at  ScienceDirect  Journal of Psychiatric Research journal homepage:  www.elsevier.com/locate/psychires http://dx.doi.org/10.1016/j.jpsychires.2015.07.013 0022-3956/© 2015 Elsevier Ltd. All rights reserved.  Journal of Psychiatric Research 68 (201 5) 270e282

documento cientifico de la Yoga.pdf

Embed Size (px)

Citation preview

Page 1: documento cientifico de la Yoga.pdf

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

7262019 documento cientifico de la Yogapdf

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 213

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

7262019 documento cientifico de la Yogapdf

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 313

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

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 413

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 2: documento cientifico de la Yoga.pdf

7262019 documento cientifico de la Yogapdf

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 213

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

7262019 documento cientifico de la Yogapdf

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 313

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

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 413

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 3: documento cientifico de la Yoga.pdf

7262019 documento cientifico de la Yogapdf

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 313

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

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 413

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 4: documento cientifico de la Yoga.pdf

7262019 documento cientifico de la Yogapdf

httpslidepdfcomreaderfulldocumento-cientifico-de-la-yogapdf 413

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 5: documento cientifico de la Yoga.pdf

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 6: documento cientifico de la Yoga.pdf

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 7: documento cientifico de la Yoga.pdf

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 8: documento cientifico de la Yoga.pdf

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

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 9: documento cientifico de la Yoga.pdf

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

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282278

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 10: documento cientifico de la Yoga.pdf

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 11: documento cientifico de la Yoga.pdf

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

References

Abercrombie HC et al 1998 Metabolic rate in the right amygdala predictsnegative affect in depressed patients Neuroreport 9 (14) 3301e3307

Ashman SB et al 2002 Stress hormone levels of children of depressed mothersDev Psychopathol 14 (2) 333e349

Australian Sports Commission tSRGS 2010 Participation in Exercise Recreationand Sport in Australia The Australian Government

Autry AE Monteggia LM 2012 Brain-derived neurotrophic factor and neuro-psychiatric disorders Pharmacol Rev 64 (2) 238e258

Avenevoli S et al 2001 Comorbidity of depression in children and adolescentsmodels and evidence from a prospective high-risk family study Biol Psychiatry49 (12) 1071e1081

Badrick E Kirschbaum C Kumari M 2007 The relationship between smokingstatus and cortisol secretion J Clin Endocrinol Metabolism 92 (3) 819e824

Balasubramaniam M Telles S Doraiswamy PM 2012 Yoga on our minds asystematic review of yoga for neuropsychiatric disorders Front Psychiatry 3117

Baldwin DS et al 2002 Can we distinguish anxiety from depression Psycho-pharmacol Bull 36 (Suppl 2) 158e165

Banasik J et al 2011 Effect of Iyengar yoga practice on fatigue and diurnal salivarycortisol concentration in breast cancer survivors J Am Acad Nurse Pract 23(3) 135e142

Banerjee B et al 2007 Effects of an integrated yoga program in modulatingpsychological stress and radiation-induced genotoxic stress in breast cancerpatients undergoing radiotherapy Integr Cancer Ther 6 (3) 242e250

Berk M et al 2011 Pathways underlying neuroprogression in bipolar disorderfocus on in1047298ammation oxidative stress and neurotrophic factors NeurosciBiobehav Rev 35 (3) 804e817

Bouayed J Rammal H Soulimani R 2009 Oxidative stress and anxiety rela-tionship and cellular pathways Oxidative Med Cell Longev 2 (2) 63e67

Bowden D et al 2012 A comparative randomised controlled trial of the effects of brain wave vibration training iyengar yoga and mindfulness on mood well-being and salivary cortisol Evid Based Complement Altern Med 2012

234713Boyer P 2000 Do anxiety and depression have a common pathophysiological

mechanism Acta Psychiatr Scand Suppl (406) 24e29Buijs RM 2013 The autonomic nervous system a balancing act Handb Clin

Neurol 117 1e11Butler LD et al 2008 Meditation with yoga group therapy with hypnosis and

psychoeducation for long-term depressed mood a randomized pilot trial J Clin Psychol 64 (7) 806e820

Capuron L Dantzer R 2003 Cytokines and depression the need for a newparadigm Brain Behav Immun 17 (Suppl 1) S119eS124

Capuron L et al 2002 Neurobehavioral effects of interferon-alpha in cancer pa-tients phenomenology and paroxetine responsiveness of symptom di-mensions Neuropsychopharmacology 26 (5) 643e652

Capuron L et al 2005 Anterior cingulate activation and error processing duringinterferon-alpha treatment Biol Psychiatry 58 (3) 190e196

Capuron L Miller AH 2004 Cytokines and psychopathology lessons frominterferon-alpha Biol Psychiatry 56 (11) 819e824

Chandwani KD et al 2014 Randomized controlled trial of yoga in women with

breast cancer undergoing radiotherapy J Clin Oncol 32 (10) 1058e

1065

MC Pascoe IE Bauer Journal of Psychiatric Research 68 (2015) 270e 282280

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

Page 12: documento cientifico de la Yoga.pdf

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

Page 13: documento cientifico de la Yoga.pdf

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