Yoga for breast cancer patients and survivors - CiteSeerX

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RESEARCH ARTICLE Open Access Yoga for breast cancer patients and survivors: a systematic review and meta-analysis Holger Cramer * , Silke Lange, Petra Klose, Anna Paul and Gustav Dobos Abstract Background: Many breast cancer patients and survivors use yoga to cope with their disease. The aim of this review was to systematically assess and meta-analyze the evidence for effects of yoga on health-related quality of life and psychological health in breast cancer patients and survivors. Methods: MEDLINE, PsycInfo, EMBASE, CAMBASE, and the Cochrane Library were screened through February 2012. Randomized controlled trials (RCTs) comparing yoga to controls were analyzed when they assessed health-related quality of life or psychological health in breast cancer patients or survivors. Risk of bias was assessed using the Cochrane risk of bias tool. Standardized mean differences (SMD) and 95% confidence intervals (CI) were calculated. Results: Twelve RCTs with a total of 742 participants were included. Seven RCTs compared yoga to no treatment; 3 RCTs compared yoga to supportive therapy; 1 RCT compared yoga to health education; and 1 RCT compared a combination of physiotherapy and yoga to physiotherapy alone. Evidence was found for short-term effects on global health-related quality of life (SMD = 0.62 [95% CI: 0.04 to 1.21]; P = 0.04), functional (SMD = 0.30 [95% CI: 0.03 to 0.57), social (SMD = 0.29 [95% CI: 0.08 to 0.50]; P < 0.01), and spiritual well-being (SMD = 0.41 [95% CI: 0.08; 0.74]; P = 0.01). These effects were, however, only present in studies with unclear or high risk of selection bias. Short-term effects on psychological health also were found: anxiety (SMD = -1.51 [95% CI: -2.47; -0.55]; P < 0.01), depression (SMD = -1.59 [95% CI: -2.68 to -0.51]; P < 0.01), perceived stress (SMD = -1.14 [95% CI:-2.16; -0.12]; P = 0.03), and psychological distress (SMD = -0.86 [95% CI:-1.50; -0.22]; P < 0.01). Subgroup analyses revealed evidence of efficacy only for yoga during active cancer treatment but not after completion of active treatment. Conclusions: This systematic review found evidence for short-term effects of yoga in improving psychological health in breast cancer patients. The short-term effects on health-related quality of life could not be clearly distinguished from bias. Yoga can be recommended as an intervention to improve psychological health during breast cancer treatment. Keywords: Breast neoplasms, Yoga, Complementary therapies, Quality of life, Psychological health, Meta-analysis, Review Background Breast cancer is the most frequent cancer in women worldwide with more than 1.5 million new cases in 2008. Twenty-three percent of all female cancer cases were diagnosed with breast cancer [1]. Due to improved diagnosis and treatment, there is a continuous increase in survival rates [2]. However, cancer patients often ex- perience side effects during treatment [3]. Many of them are bothered by reduced health-related quality of life and decreased psychological health that may persist even after the end of active treatment [4]. Depression and anxiety are the most common psychological complaints in cancer patients and survivors [5] and may arise from psychological distress; this is the inability to cope with the stress of cancer symptoms and treatment [6]. Sub- stantial psychological distress is present in 1 of every 3 breast cancer patients [3]. Psychosocial problems can ag- gravate symptom burden and seriously affect health- related quality of life [7]. Health-related quality of life describes the general well-being or global health of a * Correspondence: [email protected] Chair of Complementary and Integrative Medicine, University of Duisburg-Essen, Knappschafts-Krankenhaus, Am Deimelsberg 34a, 45276 Essen, Germany © 2012 Cramer et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Cramer et al. BMC Cancer 2012, 12:412 http://www.biomedcentral.com/1471-2407/12/412

Transcript of Yoga for breast cancer patients and survivors - CiteSeerX

Cramer et al. BMC Cancer 2012, 12:412http://www.biomedcentral.com/1471-2407/12/412

RESEARCH ARTICLE Open Access

Yoga for breast cancer patients and survivors:a systematic review and meta-analysisHolger Cramer*, Silke Lange, Petra Klose, Anna Paul and Gustav Dobos

Abstract

Background: Many breast cancer patients and survivors use yoga to cope with their disease. The aim of this reviewwas to systematically assess and meta-analyze the evidence for effects of yoga on health-related quality of life andpsychological health in breast cancer patients and survivors.

Methods: MEDLINE, PsycInfo, EMBASE, CAMBASE, and the Cochrane Library were screened through February 2012.Randomized controlled trials (RCTs) comparing yoga to controls were analyzed when they assessed health-relatedquality of life or psychological health in breast cancer patients or survivors. Risk of bias was assessed using theCochrane risk of bias tool. Standardized mean differences (SMD) and 95% confidence intervals (CI) were calculated.

Results: Twelve RCTs with a total of 742 participants were included. Seven RCTs compared yoga to no treatment; 3RCTs compared yoga to supportive therapy; 1 RCT compared yoga to health education; and 1 RCT compared acombination of physiotherapy and yoga to physiotherapy alone. Evidence was found for short-term effects onglobal health-related quality of life (SMD= 0.62 [95% CI: 0.04 to 1.21]; P = 0.04), functional (SMD= 0.30 [95% CI: 0.03to 0.57), social (SMD= 0.29 [95% CI: 0.08 to 0.50]; P < 0.01), and spiritual well-being (SMD= 0.41 [95% CI: 0.08; 0.74];P = 0.01). These effects were, however, only present in studies with unclear or high risk of selection bias. Short-termeffects on psychological health also were found: anxiety (SMD=−1.51 [95% CI: -2.47; -0.55]; P < 0.01), depression(SMD=−1.59 [95% CI: -2.68 to −0.51]; P < 0.01), perceived stress (SMD=−1.14 [95% CI:-2.16; -0.12]; P = 0.03), andpsychological distress (SMD=−0.86 [95% CI:-1.50; -0.22]; P < 0.01). Subgroup analyses revealed evidence of efficacyonly for yoga during active cancer treatment but not after completion of active treatment.

Conclusions: This systematic review found evidence for short-term effects of yoga in improving psychologicalhealth in breast cancer patients. The short-term effects on health-related quality of life could not be clearlydistinguished from bias. Yoga can be recommended as an intervention to improve psychological health duringbreast cancer treatment.

Keywords: Breast neoplasms, Yoga, Complementary therapies, Quality of life, Psychological health, Meta-analysis,Review

BackgroundBreast cancer is the most frequent cancer in womenworldwide with more than 1.5 million new cases in2008. Twenty-three percent of all female cancer caseswere diagnosed with breast cancer [1]. Due to improveddiagnosis and treatment, there is a continuous increasein survival rates [2]. However, cancer patients often ex-perience side effects during treatment [3]. Many of them

* Correspondence: [email protected] of Complementary and Integrative Medicine, University ofDuisburg-Essen, Knappschafts-Krankenhaus, Am Deimelsberg 34a, 45276Essen, Germany

© 2012 Cramer et al.; licensee BioMed CentralCommons Attribution License (http://creativecreproduction in any medium, provided the or

are bothered by reduced health-related quality of lifeand decreased psychological health that may persist evenafter the end of active treatment [4]. Depression andanxiety are the most common psychological complaintsin cancer patients and survivors [5] and may arise frompsychological distress; this is the inability to cope withthe stress of cancer symptoms and treatment [6]. Sub-stantial psychological distress is present in 1 of every 3breast cancer patients [3]. Psychosocial problems can ag-gravate symptom burden and seriously affect health-related quality of life [7]. Health-related quality of lifedescribes the general well-being or global health of a

Ltd. This is an Open Access article distributed under the terms of the Creativeommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andiginal work is properly cited.

Table 1 Complete search strategy for Medline

Concept Search strategy

Yoga (yoga[MeSH Terms] OR yog*[Title/Abstract])

AND

Health-relatedquality of life orpsychological health

(quality of life[MeSH Terms] OR quality oflife[Title/Abstract] OR well-being[Title/Abstract]OR mental health[MeSH Terms] OR mentalhealth[Title/Abstract] OR psychologicalhealth[Title/Abstract] OR anxiety[MeSH Terms]OR anxiety[Title/Abstract] OR depressivedisorder[MeSH Terms] OR depression[Title/Abstract] OR stress[Title/Abstract] ORdistress[Title/Abstract] OR affect[MeSH Terms]OR mood[Title/Abstract])

AND

Breast cancer (breast neoplasms[MeSH Terms] OR (breast[Title/Abstract] AND (neoplasms[Title/Abstract] ORcancer[Title/Abstract] OR oncology[Title/Abstract])))

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person and consists of a variety of dimensions includingphysical, mental, and spiritual well-being, role function-ing and social support [7].In order to cope with the disease, many breast cancer

patients and survivors use complementary medicine [8]and yoga is among the most commonly used comple-mentary treatments for breast cancer-related impair-ments [8]. Derived from ancient Indian philosophy, yogacomprises advice for ethical lifestyle, as well as spiritualpractice and physical postures, with the ultimate goal ofuniting mind, body and spirit [9]. In North America andEurope, yoga is most often associated with physical exer-cises (asanas), breathing techniques (pranayama) andmeditation (dyana) [10]. An estimated 15 million Americanadults report having practiced yoga at least once in theirlifetime, almost half of those using yoga explicitly forcoping with disease or promoting health [11].Previously, meta-analyses concluded that conventional

physical activity can improve quality of life in breast can-cer patients and survivors [12-14]. However, while sys-tematic reviews and meta-analyses have shown similarresults for yoga in heterogeneous cancer groups [15,16],there is no meta-analysis on yoga for breast cancerpatients or survivors yet. Since patients with differenttypes of cancer are heterogeneous in terms of socio-demographic factors, symptoms, treatment and sideeffects, meta-analyses should focus on homogenous can-cer groups [12].This systematic review focused on the effect of yoga

on health-related quality of life and psychological healthin breast cancer patients and survivors.

MethodsPRISMA guidelines for systematic reviews and meta-analyses [17] and the recommendations of the CochraneCollaboration [18] were followed.

Literature searchPubmed/Medline, EMBASE, the Cochrane Library,PsycINFO, and CAMBASE were searched from their in-ception until February 2012 without language restrictions.Search terms for yoga were combined with search termsfor health-related quality of life or psychological health andwith search terms for breast cancer. The search strategywas adapted for each database as necessary. The completesearch strategy for Pubmed/Medline is shown in Table 1.Reference lists of identified original and review papers alsowere reviewed. Additionally, the table of contents of theInternational Journal of Yoga Therapy was reviewed.Abstracts identified during literature search were

screened by 3 authors independently. Retrieved articleswere read in full by 3 authors to determine whether theymet the eligibility criteria.

Inclusion criteriaTo be eligible, studies had to meet the followingconditions:

1) Types of studies. Randomized controlled trials (RCTs)were eligible. Studies were eligible only if they werepublished as full paper.

2) Types of participants. Studies of adult (older than18 years) patients with a history of breast cancerwere eligible.

3) Types of interventions. Studies that compared yogawith no treatment or any active treatment wereeligible. Studies were excluded if yoga was not themain intervention but a part of a multimodalintervention, such as mindfulness-based stressreduction (for a meta-analysis of mindfulness-basedstress reduction for breast cancer patients andsurvivors see [19]). No restrictions were maderegarding yoga tradition, length, frequency orduration of the program. Co-interventions wereallowed.

4) Types of outcome measures. Studies were eligible ifthey assessed health-related quality of life or well-being (global health-related quality of life, mental,physical, functional, social, and/or spiritual well-being) and/or psychological health (depression,anxiety, perceived stress, and/or psychologicaldistress). If available, safety data served as secondaryoutcome measures.

Data extractionThree reviewers independently extracted data on charac-teristics of the study (e.g. trial design, randomization,blinding), characteristics of the patient population (e.g.sample size, stage of cancer, current treatment, age),characteristics of the intervention and control (e.g. type,

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program length, frequency and duration), outcome mea-sures and results.

Risk of bias in individual studiesRisk of bias was assessed by 2 authors independentlyusing the Cochrane risk of bias tool [18]. This toolassesses risk of bias on the following domains: selectionbias, performance bias, detection bias, attrition bias,reporting bias, and other bias. Discrepancies wererechecked with a third reviewer and consensus achievedby discussion.

Data analysisStudies were analyzed separately for short-term andlong-term follow-ups. For the purpose of this review,short-term follow-up was defined as outcome measurestaken closest to the end of the intervention and long-term follow-up as measures taken closest to 12 monthsafter randomization [20].

Assessment of overall effect sizeIf at least two studies were available on a specific out-come, data for this outcome was included in the meta-analysis. Overall effects were analyzed using ReviewManager 5 software (Version 5.1, The Nordic CochraneCentre, Copenhagen). A random effects model was usedbecause it involves the assumption of statistical hetero-geneity between studies [18].As a specific outcome could be measured on different

scales, standardized mean differences (SMD) with 95%confidence intervals (CI) were calculated. SMD was cal-culated as the difference in means between groupsdivided by the pooled standard deviation. Where nostandard deviations were available, they were calculatedfrom standard errors, confidence intervals or t values[18], or attempts were made to obtain the missing datafrom the trial authors by email. The effect size used inthis review is also known in social science as Hedges'(adjusted) g. Cohen's categories were used to evaluatethe magnitude of the effect size with small, moderateand large effect sizes being defined as SMD=0.2 to 0.5,SMD=0.5 to 0.8 and SMD>0.8, respectively [21].A positive SMD was defined to indicate beneficial

effects of yoga compared to the control intervention forhealth-related quality of life (e.g. increased well-being),while a negative SMD was defined to indicate beneficialeffects for the other outcomes (e.g. decreased depres-sion). If necessary, scores were inverted by subtractingthe mean from the maximum score of the instrument[18].

Assessment of heterogeneityHeterogeneity was explored using the I2 statistics, ameasure of how much variance between studies can be

attributed to differences between studies rather thanchance. I2 > 50% was regarded to indicate strong hetero-geneity [18]. The Chi2 test was used to assess whetherdifferences in results are compatible with chance alone.Since this test has low power when only few studies orstudies with low sample size are included in a meta-analysis, a p value ≤ 0.10 was regarded to indicate sig-nificant heterogeneity [18].

Subgroup and sensitivity analysesBesides assessment of overall effect, subgroup analyseswere conducted for type of yoga intervention (yoga in-cluding physical activity/asanas; yoga not includingphysical activity/asanas) and for type of control interven-tion (yoga versus no treatment; yoga versus active com-parator). Moreover, subgroup analyses were conductedfor current treatment status (patients who were under-going active cancer treatment; patients who had com-pleted active treatment).To test the robustness of significant results, sensitivity

analyses were conducted for studies with high or unclearrisk of selection bias (inadequate or unclear random se-quence generation and/or allocation concealment) ver-sus low risk of selection bias (adequate randomsequence generation and/or allocation concealment).If statistical heterogeneity was present in the respective

meta-analysis, subgroup and sensitivity analyses werealso used to explore possible reasons for heterogeneity.

Risk of bias across studiesPublication bias was assessed by visual analysis of funnelplots, generated using Review Manager 5 software. Fun-nel plots were analyzed only if at least 10 studies wereincluded in a meta-analysis. Roughly symmetrical funnelplots were regarded to indicate low risk while asymmet-rical funnel plots were regarded to indicate high risk ofpublication bias [22].

ResultsStudy selectionThe literature search generated a total of 156 records, 54of them were duplicates (Figure 1). Three additionalrecords were found in the International Journal of YogaTherapy. Eighteen full-text articles were assessed for eli-gibility [23-40] and 6 were excluded. One articlereported effects of yoga in patients with mixed types ofcancer, not just breast cancer [37]; 1 article did not as-sess health-related quality of life or psychological healthbut natural killer cell counts [38]; 2 articles [39,40]reported a subgroup analysis of an already publishedtrial [33]. Three articles reported different outcomes of 1single trial; these articles were treated as 1 single study[34-36]. Hence, this was regarded as 1 included articleand 2 excluded articles. Twelve RCTs, involving a total

156 of records identified through database searching- 41 Pubmed- 18 Cochrane- 87 Embase- 0 Cambase- 10 PsycInfo

3 of additional records identified through other sources

- 3 International Journal of Yoga Therapy

87 of records excluded

6 of full-text articles excluded-1 heterogeneous cancer population-1 neither quality of life nor psychological health-2 multiple publications on the same sample-2 subsample of already published data

10 of studies included in quantitative synthesis

(meta-analysis)

2 of full-text articles excluded-2 insufficient raw data

105 of records after duplicates removed

18 of full-text articles assessed for eligibility

12 of studies included in qualitative synthesis

Figure 1 Flowchart of the results of the literature search.

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of 742 patients, were included in the qualitative synthe-sis [23-36]. One RCT did not report any group compari-sons but presented effects of the yoga intervention in amore qualitative way and therefore was not included inthe meta-analysis [25]. One RCT did not report standarddeviations, standard errors, confidence intervals, or t-values [27]. Since the missing data could not be obtainedfrom the authors of the respective study by email, thisstudy was excluded from the meta-analysis. Finally, 10studies were included in the meta-analysis.

Study characteristicsStudy characteristics are shown in Table 2.

Setting and participant characteristicsEight studies originated from North America[23,25-29,31,32], 1 from Europe [30] and 3 from India[24,33-36]. Participants mainly were recruited from can-cer centers [23-25,27-30,32-36], but also from privateclinics [32], tumor registries [26], and newspaper orwebsite advertisements [26,31].Participants in 5 studies were receiving active cancer

treatment (i.e. chemotherapy, radiotherapy, or both)

during the yoga intervention [24,28,30,33-36], partici-pants in 5 studies had completed active treatment beforethe onset of the study [23,25-27,31] and 2 studies did in-clude both participants receiving active cancer treatmentand those who did not [29,32]. Stage of cancer wasmixed, however, only 2 studies included patients withstage 4 breast cancer [23,29] and only 3 studies includedpatients with stage 0 breast cancer [28,29,31]. Partici-pants’ mean age ranged from 44 years to 63 years; be-tween 0% and 100% of participants in each study wereCaucasians. One study explicitly strived to include amultiethnic sample [32].Yoga interventions were heterogeneous and included

an integrated yoga program [24,33-36], Iyengar yoga[23,25,26], Yoga of Awareness [27], Viniyoga [31], re-storative yoga [29], yoga based on Patanjali‘s yoga trad-ition [28], Yoga in daily lifeW [30], and hatha yoga [32].Program length and intensity varied, ranging from dailyinterventions over 1 week [30] to one intervention perweek over 6 months [31]. All but 1 RCT [30] includedphysical activity/asanas in their yoga intervention. Con-trol groups were wait-listed and did not receive anytreatment in 7 studies [23,25,27-29,31,32]; received brief

Table 2 Characteristics of the included studies

Authors, year No. ofpatients

Meanage

Statusofcancer

Currenttreatment

Treatmentgroup:Intervention

Controlgroup:Intervention

OutcomemeasuresOutcomeassessment

Results

Programlength,frequency,duration

Programlength,frequency,duration

a) Short-termfollow-upb) Long-termfollow-up

Banasik et al.,2011 [23]

18 62.9 II-IV At least 2monthpost-treatment

Iyengar Yoga:yoga postures

Wait-list, notreatment

Health-relatedquality of life (FACT-B)

No significanteffects.

8 weeks, twiceweekly, 90 minutes

8 weeks a) Week 8b) NA

Banerjee et al.,2007 [24]

68 44 II-III Radiotherapy Integrated yogaprogram: yogapostures, deeprelaxation,breathingtechniques,meditation,guided imagery,group awareness

Supportivecounseling andadvice to takelight exercise

Anxiety (HADS) Significant short-term effects onanxiety (p < 0.001),depression (p < 0.001),perceived stress(p < 0.001).

6 weeks, frequencyNR, 90 minutes

6 weeks, frequencyand duration NR

Depression (HADS)Perceivedstress (PSS)a) Week 6b) NA

Blank et al.,2003 [25]

18 NR I-III Antiestrogenor aromataseinhibitor, atleast 8 weekspost-chemotherapy

Iyengar yoga: yogapostures, deeprelaxation, meditation,chanting

Wait-list, notreatment

Questionnaireregardingperceived stress,psychologicaloutcomes

No group comparison.

8 weeks, twiceweekly, duration NR

8 weeks a) Week 6b) NA

Bower et al.,2011 [26]

31 53.9 0-II No localand/oradjuvantcancertherapy

Iyengar yoga: postures,breathing techniques

Health education Vitality (SF-36) Significant short-termeffects on depression(p = 0.026).

12 weeks, twiceweekly, 90 minutes

12 weeks, onceweekly, 120minutes

Depression (BDI)

Clinically importantlong-term effectson vitality.

Perceivedstress (PSS)a) weeks12 to 14b) week 24

Carson et al.,2009 [27]

37 54.4 I-II No currentchemotherapyor hormonereplacementtherapy

Yoga of Awareness:yoga postures,breathing techniques,meditation, study ofpertinent topics,group discussion

Wait-list, notreatment

Daily diaryregardingnegative mood,symptom-related distress

Significant short-termeffects on symptom-related distress(p < 0.0001).

8 weeks, onceweekly, 120 minutes

8 weeks a) Week 6 Significant long-termeffects on symptom-related distress(p < 0.0001) andnegative mood(p < 0.0001).

b) Week 20

Chandwaniet al., 2010 [28]

81 NR 0-III Radiotherapy Yoga based onPatanjali`s yogasutras: yoga postures,deep relaxation,breath control,meditation

Wait-list, notreatment

Health-relatedquality of life(SF-36)

Significant short-termeffects on SF-36physical componentscore (p = 0.04),general health(p = 0.005), physicalfunction (p = 0.04).

6 weeks, twiceweekly, 60 minutes

6 weeks

Depression (CES-D)

No significant long-term effects.

Anxiety (STAI)Intrusion/avoidance (IES)a) Week 7b) Week 18

Danhauer et al.,2009 [29]

44 55.8 Any Any Restorative yoga:yoga postures,breathing techniques,deep relaxation,meditation

Wait-list, notreatment

Health-related qualityof life (FACT-B,FACIT-Sp, SF-12)

Significant short-term effects onmental well-being(p = 0.004), spiritualwell-being (p = 0.0009),depression (p = 0.026),positive affect(p = 0.01).

10 weeks, onceweekly, 75 minutes

10 weeks

Depression (CES-D)Positive and negativeaffect (PANAS)a) Week 10b) NA

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Table 2 Characteristics of the included studies (Continued)

Kovačič & Kovačič,2011 [30]

32 NR I-II Radiotherapy,chemotherapy

Yoga in Daily LifeW

System: breathingtechniques, deeprelaxation, progressivemuscle relaxation,meditation

Standardphysiotherapy

Mental well-being(GHQ-12)

Significant short-termeffects on mentalwell-being (p < 0.0005),perceived stress(p < 0.0005).

1 week, 7 times aweek, 45 minutes

1 week

Psychologicaldistress (RSCL)

Significant long-termeffects on mentalwell-being (p < 0.0005),psychological distress(p < 0.0005), perceivedstress (p < 0.0005).

Standardphysiotherapy

Perceivedstress (PSS)

1 week

a) Week 2b) Week 5

Littman et al.,2011 [31]

63 60.6 0-III At least 3monthpost-treatment

Viniyoga: yogapostures, breathingtechniques, deeprelaxation, meditation

Wait-list, notreatment

Health-relatedquality of life(FACT-B)

No significant effects.

6 months, 1 to 3times a week75 minutes

6 month a) Week 48b) NA

Moadel et al.,2007 [32]

164 54.81 I-III Any Hatha yoga: yogapostures, breathing,techniques,meditation

Wait-list, notreatment

Health-relatedquality of life(FACT-G, FACIT-Sp)

Significant short-termeffect on socialwell-being (p < 0.018).

12 weeks, onceweekly, 90 minutes

12 weeksAnxiety (DistressedMood Index)Psychologicaldistress (DistressedMood Index)a) Week 12b) Week 24 (NR)

Raghavendraet al., 2007 [33]

98 NR II-III Chemotherapy Integrated yogaprogram: yogapostures, breathingtechniques, relaxationwith imagery,chanting

Brief supportivetherapy

Health-relatedquality of life (FLIC)

Significant short-termeffects on overallhealth-related qualityof life (p < 0.001),anxiety (p < 0.001),depression (p < 0.001),symptom distress(p < 0.001).

Program length NR,30 minutes 4 times,60 minutes every10 days

Program lengthNR, 60 minutesonce, 30 minutesevery 10 days

Anxiety (STAI)Depression (BDI)Symptom distress(SubjectiveSymptom Checklist)a) NRb) NA

Vadiraja et al.,2009 [34-36]

88 47.23 II-III Radiotherapy Integrated yogaprogram: yogapostures, breathingtechniques, relaxationwith imagery,meditation

Brief supportivetherapy

Health-relatedquality of life(EORTCQLQ-C30)Anxiety (HADS)Depression(HADS)Positive andnegative affect(PANAS)

Significant short-termeffects on emotionalfunction (p = 0.001),cognitive function(p = 0.03), anxiety(p < 0.001), depression(p = 0.002), positiveaffect (p = 0.007),negative affect(p < 0.001), perceivedstress (p < 0.001),psychological distress(p < 0.001).

6 weeks, 60 minutesat least 3 times aweek (18–24 sessionin total)

6 weeks, 15minutes every10 days (3–4sessions in total)

Perceivedstress (PSS)Psychologicaldistress (RSCL)a) Week 6b) NA

Abbreviations: BDI: Beck’s Depression Inventory; CES-D: Center of Epidemiologic Studies Depression Scale; EORTC QLQ-C30: European Organisation for Researchand Treatment of Cancer Quality of Life Questionnaire C30; FACT: Functional Assessment of Cancer Therapy (B: Breast; G: General; Sp: Spirituality); FLIC: FunctionalLiving Index for Cancer; GHQ-12: General Health Questionnaire-12; HADS: Hospital Anxiety and Depression Scale; IES: Impact of Events Scale; PANAS: Positive &negative affect schedule; PSS: support cancer care; RSCL: Rotterdam Symptom Checklist; STAI: State Trait Anxiety Inventory; SF-36/-12: Medical Outcomes Study 36/12-item short-form survey; NA: not applicable; NR: not reported.

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supportive therapy or counseling in 3 studies [24,33-36];or received health education classes in 1 study [26]. Onestudy compared yoga combined with physiotherapy tophysiotherapy alone [30]. No study exactly matched pro-gram length, frequency and duration of the controlintervention with the yoga intervention.

Outcome measuresHealth-related quality of life Group comparisons forhealth-related quality of life were reported in 8 studies[23,28-36]. Functional Assessment of Cancer Therapy-General was used in 1 study [32], Functional Assessmentof Cancer Therapy-Breast was used in 3 studies [23,29,31],and Functional Assessment of Chronic Illness Therapy-Spirituality was used in 2 studies [29,32]. MedicalOutcomes Study 36-item short-form survey [28], MedicalOutcomes Study 12-item short-form survey [29], Func-tional Living Index for Cancer [33], General HealthQuestionnaire-12 [30] and European Organization forResearch and Treatment of Cancer Quality of LifeQuestionnaire C30 [35] were used in 1 study each.

Psychological health Eight studies reported groupdifferences for measures of psychological health[24,26,28-30,32-36]. Of the 5 studies that assessedanxiety, 2 used the Hospital Anxiety and Depression Scale[24,34-36], 2 used the State Trait Anxiety Inventory[28,33], and 1 used the Distressed Mood Index [32]. De-pression was assessed in 6 studies. Two studies used theHospital Anxiety and Depression Scale [24,34-36], 2 usedthe Center of Epidemiologic Studies Depression Scale[28,29], and 2 used the Becks Depression Inventory [26,33].Perceived stress was assessed in 4 studies, all usingthe Perceived Stress Scale [24,26,30,34-36]. Six studiesassessed psychological distress, 1 of those used the

Table 3 Risk of bias assessment of the included studies using

Bias Randomsequencegeneration(selection bias)

Allocationconcealment(selection bias)

Blindingparticipaand pers(perform

Authors, year

Banasik et al., 2011 [23] Unclear Unclear High risk

Banerjee et al., 2007 [24] Low risk Low risk High risk

Blank et al., 2003 [25] Unclear Unclear High risk

Bower et al., 2011 [26] Low risk Low risk High risk

Carson et al., 2009 [27] Low risk Low risk High risk

Chandwani et al., 2010 [28] Low risk Unclear High risk

Danhauer et al., 2009 [29] Unclear Unclear High risk

Kovačič & Kovačič, 2011 [30] Low risk Low risk Low risk

Littman et al., 2011 [31] Low risk Unclear High risk

Moadel et al., 2007 [32] Unclear Unclear High risk

Raghavendra et al., 2007 [33] Low risk Low risk High risk

Vadiraja et al., 2009 [34-36] Low risk Low risk High risk

Rotterdam Symptom Check List [30], 2 used the Positiveand Negative Affect Scale [29,34-36], 1 used the DistressedMood Index [32], 1 used the impact of event scale [28],and 1 used the Subjective Symptom Checklist [33].

Risk of bias in individual studiesRisk of bias for each study is shown in Table 3. No studyfulfilled all criteria. Generally, risk of selection bias washigh; 6 out of 12 studies did not report adequate randomsequence generation and/or allocation concealment[23,25,28,29,31,32]. While no study reported blinding ofpatients or yoga providers, 1 study reported blinding ofall health care providers and involved personnel [30].Outcome assessors were blinded to treatment allocationin 3 studies [26,27,30]. Four studies had high risk of at-trition bias due to high and/or unbalanced drop-outrates [24,25,33-36] and 2 studies had high risk of select-ive reporting bias [25,34-36]. One study was judged tohave high risk of other bias, since no outcomes werereported for the control group and no formal statisticswere conducted [25].

Analyses of overall effectsHealth-related quality of lifeMeta-analysis revealed evidence for a moderate short-term effect of yoga on global health-related quality of life(SMD=0.62; 95% CI: 0.04 to 1.21; P = 0.04). There wasno evidence for improved mental (SMD=0.45; 95% CI:-0.06 to 0.96; P = 0.08) or physical well-being (SMD=0.45; 95% CI: -0.19 to 1.08; P = 0.17) at the short-term.Significant small short-term effects were found favoringthe yoga groups for functional (SMD=0.30; 95% CI: 0.03to 0.57; P = 0.03), social (SMD=0.29; 95% CI: 0.08 to0.50; P < 0.01) and spiritual well-being (SMD=0.41; 95%CI: 0.08 to 0.74; P = 0.01) (Figure 2). At long-term

the Cochrane risk of bias tool

ofntsonnelance bias)

Blinding ofoutcomeassessment(detection bias)

Incompleteoutcome data(attrition bias)

Selectivereporting(reportingbias)

Other bias

Unclear Low risk Low risk Low risk

Unclear High risk Low risk Low risk

Unclear High risk High risk High risk

Low risk Low risk Low risk Low risk

Low risk Low risk Low risk Low risk

Unclear Low risk Low risk Low risk

Unclear Low risk Low risk Low risk

Low risk Unclear Low risk Low risk

High risk Low risk Low risk Low risk

Unclear Low risk Low risk Low risk

Unclear High risk Low risk Low risk

Unclear High risk High risk Low risk

Cramer et al. BMC Cancer 2012, 12:412 Page 8 of 13http://www.biomedcentral.com/1471-2407/12/412

follow-up, there was no evidence for improved mentalwell-being (SMD=2.36; 95% CI: -2.02 to 6.74; P = 0.29)(Figure 2).

Psychological healthEvidence for large short-term effects was found for anx-iety (SMD=−1.51; 95% CI: -2.47 to −0.55; P < 0.01), de-pression (SMD=−1.59; 95% CI: -2.68 to −0.51; P < 0.01),perceived stress (SMD=−1.14; 95% CI: -2.16 to −0.12;P = 0.03), and psychological distress (SMD=−0.86; 95%CI: -1.50 to −0.22; P < 0.01) (Figure 3). The effects on de-pression (SMD=−0.36; 95% CI: -0.80 to 0.07; P = 0.10),perceived stress (SMD=−1.76; 95% CI: -5.08 to 1.56;P = 0.14) and psychological distress (SMD=−1.73; 95%CI: -4.02 to 0.56; P = 0.14) were not maintained at thelong-term follow-up (Figure 3).

SafetyThree studies reported adverse events [26,29,31]. Only 1adverse event was reported (out of 138 patients): 1 par-ticipant experienced a transient back spasm during class[26]. The other 2 studies stated that no adverse eventswere reported [29,31].

Subgroup analysesThe results did not change substantially when only stud-ies that included physical activity/asanas in their yogaintervention were considered [23-29,31-36]. As only 1study did not include physical activity/asanas [30], noseparate analysis was conducted.When comparing yoga to no treatment, small short-

term effects were found for global quality of life, func-tional, social, and spiritual well-being, but not for mentalwell-being, physical well-being, anxiety, depression, andpsychological distress (Table 4). When comparing yogato an active control intervention, evidence for largeshort-term effects was found for mental well-being, anx-iety, depression, perceived stress, and psychological dis-tress (Table 4).In studies in which the intervention was administered

to patients who were undergoing active treatment[24,28,30,33-36], no evidence for short-term effects wasfound for mental, physical, or social, well-being. Evi-dence for large short-term effects was found for anxiety,depression, perceived stress, and psychological distress(Table 5). For studies in which the participants had com-pleted active treatment [23,25-27,31], meta-analyses on2 RCTs did not find any group differences in mental,physical, functional, or social well-being (Table 5).

Sensitivity analysisSensitivity analyses demonstrated a significant short-term effect on general health-related quality of life, func-tional, social, and spiritual well-being in studies with

unclear or high risk of selection bias whereas theseeffects were not significant in studies with low risk ofselection bias. Short-term effects on anxiety, depres-sion, perceived stress, and psychological distress weresignificant in studies with low risk of selection bias butnot in studies with unclear or high risk of selection bias.

Publication biasDue to the small number of eligible studies, funnel plotswere not analyzed.

DiscussionPrevious systematic reviews found favorable effects ofyoga interventions on health-related quality of life andpsychological health in cancer patients and survivors[15,16]. However, none of these reviews focused only onwomen with breast cancer.The aim of the present review was to systematically

evaluate the totality of evidence for the efficacy of yogaon health-related quality of life and psychological healthin breast cancer patients and survivors. This reviewfound a moderate size short-term effect on globalhealth-related quality of life along with small size short-term effects on functional, social, and spiritual quality oflife. Regarding psychological health, large short-termeffects on anxiety, depression, perceived stress, and psy-chological distress were found. At the moment there isno evidence for longer-term effects of yoga in breastcancer patients and survivors. More RCTs with longerfollow-ups are needed. The available safety data suggestthat yoga is not associated with serious adverse events.However, future RCTs should ensure more rigorousreporting of adverse events and reasons for drop-outs.The findings in this review are partly in line with a

previous meta-analysis on yoga for heterogeneous cancerpopulations, which reported positive effects on psycho-logical health while finding no effects in health-relatedquality of life [15]. However, meta-analyses focusing onphysical activity (not including yoga) for breast cancerpatients and survivors reported positive effects on qual-ity of life [12,13].Besides physical activity, yoga also encompasses

breathing techniques and meditation [10]. While medita-tion on its own may have a positive impact on psycho-logical health in cancer patients [19,41], studies havealso demonstrated specific positive effects of physicalyoga postures on mood [42].The finding that yoga was more effective during active

cancer treatment than after completion of cancer treat-ment is in contrast to a prior RCT, that reported morefavorable results in a subgroup of breast cancer patientsthat were not receiving chemotherapy [32]. The findingsin this meta-analysis might result from the small numberof studies that could be included in the meta-analyses

SHORT-TERM EFFECTS

LONG-TERM EFFECTS

Study

Danhauer et al., 2009

Littman et al., 2011

Moadel et al., 2010

Raghavendra et al., 2007

Total (95% CI)

Heterogeneity: Chi² = 14.48, df = 3 (P = 0.002); I² = 79%

Test for overall effect: Z = 2.08 (P = 0.04)

Mean

114.8

90.3

75.2

142.1

SD

19.1

11

18.96

10.2

Total

13

30

84

28

155

Mean

98.4

87.7

69.94

111.7

SD

31.8

15

19.39

25.5

Total

14

27

44

34

119

Weight

20.7%

25.8%

28.7%

24.8%

100.0%

IV, Random, 95% CI

0.60 [-0.17, 1.38]

0.20 [-0.32, 0.72]

0.27 [-0.09, 0.64]

1.49 [0.92, 2.06]

0.62 [0.04, 1.21]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours control Favours yoga

GENERAL QUALITY OF LIFE

Study

Banasik et al., 2011

Chandwani et al., 2010

Danhauer et al., 2009

, 2011

Littman et al., 2011

Moadel et al., 2010

Vadiraja et al., 2009

Total (95% CI)

Heterogeneity: Chi² = 32.30, df = 6 (P < 0.0001); I² = 81%

Test for overall effect: Z = 1.74 (P = 0.08)

Mean

-0.47

49.7

52.2

26.19

20.3

17.76

75.12

SD

0.36

1.7

6.6

2.97

4

5.06

21.16

Total

7

27

13

16

30

84

47

224

Mean

-0.38

49.9

47.5

16.37

20.8

16.32

59.23

SD

0.31

1.7

13.8

4.05

3.1

5.61

23.32

Total

7

31

14

16

27

44

44

183

Weight

10.4%

15.8%

13.2%

11.0%

15.7%

17.2%

16.7%

100.0%

IV, Random, 95% CI

-0.25 [-1.30, 0.80]

-0.12 [-0.63, 0.40]

0.42 [-0.35, 1.18]

2.70 [1.71, 3.68]

-0.14 [-0.66, 0.38]

0.27 [-0.09, 0.64]

0.71 [0.28, 1.13]

0.45 [-0.06, 0.96]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours control Favours yoga

MENTAL WELL-BEING

Study

Banasik et al., 2011

Chandwani et al., 2010

Danhauer et al., 2009

Littman et al., 2011

Moadel et al., 2010

Vadiraja et al., 2009

Total (95% CI)

Heterogeneity: Chi² = 38.38, df = 5 (P < 0.00001); I² = 87%

Test for overall effect: Z = 1.38 (P = 0.17)

Mean

-0.77

43.1

22.5

25.4

19.6

73.26

SD

0.94

1.8

7.6

1.7

6.65

25.33

Total

7

27

13

30

84

47

208

Mean

-0.42

39

21.1

24.3

19.26

68.96

SD

0.25

1.7

5.7

4.4

6.35

30.12

Total

7

31

14

27

44

44

167

Weight

12.8%

16.4%

15.6%

17.7%

18.9%

18.6%

100.0%

IV, Random, 95% CI

-0.48 [-1.54, 0.59]

2.32 [1.64, 2.99]

0.20 [-0.55, 0.96]

0.33 [-0.19, 0.86]

0.05 [-0.31, 0.42]

0.15 [-0.26, 0.57]

0.45 [-0.19, 1.08]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4

Favours control Favours yoga

PHYSICAL WELL-BEING

Study

Banasik et al., 2011

Danhauer et al., 2009

Littman et al., 2011

Moadel et al., 2010

Total (95% CI)

Heterogeneity: Chi² = 1.14, df = 3 (P = 0.77); I² = 0%

Test for overall effect: Z = 2.20 (P = 0.03)

Mean

3.46

21.9

22.6

17.45

SD

0.64

4.7

3.9

6.86

Total

7

13

30

84

134

Mean

3.24

17.4

21.7

15.68

SD

0.56

7.5

4.7

6.56

Total

7

14

27

44

92

Weight

6.5%

12.0%

26.9%

54.6%

100.0%

IV, Random, 95% CI

0.34 [-0.72, 1.40]

0.69 [-0.09, 1.47]

0.21 [-0.31, 0.73]

0.26 [-0.11, 0.63]

0.30 [0.03, 0.57]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-2 -1 0 1 2

Favours control Favours yoga

FUNCTIONAL WELL-BEING

Study

Banasik et al., 2011

Chandwani et al., 2010

Danhauer et al., 2009

Littman et al., 2011

Moadel et al., 2010

Vadiraja et al., 2009

Total (95% CI)

Heterogeneity: Chi² = 3.71, df = 5 (P = 0.59); I² = 0%

Test for overall effect: Z = 2.75 (P = 0.006)

Mean

2.8

84.6

23.1

22.1

20.38

54.96

SD

0.67

7.1

5

5

5.57

23.98

Total

7

27

13

30

84

47

208

Mean

3.16

80

20.4

20.9

18.67

49.93

SD

0.83

7.5

6.8

6

6.28

24.23

Total

7

31

14

27

44

44

167

Weight

3.8%

15.4%

7.4%

15.9%

32.1%

25.4%

100.0%

IV, Random, 95% CI

-0.45 [-1.51, 0.62]

0.62 [0.09, 1.15]

0.44 [-0.33, 1.20]

0.22 [-0.31, 0.74]

0.29 [-0.07, 0.66]

0.21 [-0.21, 0.62]

0.29 [0.08, 0.50]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-2 -1 0 1 2Favours control Favours yoga

SOCIAL WELL-BEING

Study

Danhauer et al., 2009

Moadel et al., 2010

Total (95% CI)

Heterogeneity: Chi² = 0.11, df = 1 (P = 0.74); I² = 0%

Test for overall effect: Z = 2.44 (P = 0.01)

Mean

26

37.4

SD

6.7

9.09

Total

13

84

97

Mean

21.5

33.55

SD

9.4

11.34

Total

14

44

58

Weight

18.6%

81.4%

100.0%

IV, Random, 95% CI

0.53 [-0.24, 1.30]

0.39 [0.02, 0.75]

0.41 [0.08, 0.74]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-2 -1 0 1 2Favours control Favours yoga

SPIRITUAL WELL-BEING

Study

Chandwani et al., 2010

, 2011

Total (95% CI)

Heterogeneity: Chi² = 34.36, df = 1 (P < 0.00001); I² = 97%

Test for overall effect: Z = 1.06 (P = 0.29)

Mean

50.9

32.44

SD

2.7

2.42

Total

27

16

43

Mean

50.4

14.87

SD

2.9

4.62

Total

29

16

45

Weight

51.1%

48.9%

100.0%

IV, Random, 95% CI

0.18 [-0.35, 0.70]

4.64 [3.25, 6.04]

2.36 [-2.02, 6.74]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours control Favours yoga

MENTAL WELL-BEING

Figure 2 Effect sizes of yoga versus controls on health-related quality of life: general quality of life, mental, physical, social, andspiritual well-being.

Cramer et al. BMC Cancer 2012, 12:412 Page 9 of 13http://www.biomedcentral.com/1471-2407/12/412

SHORT-TERM EFFECTS

Study

Banerjee et al., 2007

Chandwani et al., 2010

Moadel et al., 2010

Raghavendra et al., 2007

Vadiraja et al., 2009

Total (95% CI)

Heterogeneity: Chi² = 64.57, df = 4 (P < 0.00001); I² = 94%

Test for overall effect: Z = 3.09 (P = 0.002)

Mean

4.1

28

8.1

29.2

4.88

SD

1

2.2

7.64

3.8

3.34

Total

35

27

84

28

42

216

Mean

10.5

30.2

10.26

37.5

8.12

SD

1.8

2.4

8.08

7.6

3.8

Total

23

31

44

34

33

165

Weight

17.5%

20.4%

21.1%

20.3%

20.7%

100.0%

IV, Random, 95% CI

-4.60 [-5.62, -3.59]

-0.94 [-1.49, -0.39]

-0.28 [-0.64, 0.09]

-1.32 [-1.88, -0.77]

-0.90 [-1.38, -0.42]

-1.51 [-2.47, -0.55]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours yoga Favours control

ANXIETY

Study

Banerjee et al., 2007

Bower et al., 2011

Chandwani et al., 2010

Danhauer et al., 2009

Raghavendra et al., 2007

Vadiraja et al., 2009

Total (95% CI)

Heterogeneity: Chi² = 84.03, df = 5 (P < 0.00001); I² = 94%

Test for overall effect: Z = 2.87 (P = 0.004)

Mean

3.4

7.7

6.6

8.1

6.6

4.14

SD

0.5

5.8

2.1

8.9

4.6

3.45

Total

35

16

27

13

28

42

161

Mean

9.7

11.6

7

17.8

14.2

6.53

SD

1.2

7.1

2.2

16.9

6.6

3.78

Total

23

15

31

14

34

33

150

Weight

13.7%

16.9%

17.6%

16.7%

17.5%

17.7%

100.0%

IV, Random, 95% CI

-7.34 [-8.82, -5.86]

-0.59 [-1.31, 0.13]

-0.18 [-0.70, 0.33]

-0.69 [-1.47, 0.09]

-1.30 [-1.85, -0.74]

-0.66 [-1.13, -0.19]

-1.59 [-2.68, -0.51]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours yoga Favours control

DEPRESSION

Study

Banerjee et al., 2007

Bower et al., 2011

Vadiraja et al., 2009

Total (95% CI)

Heterogeneity: Chi² = 16.42, df = 2 (P = 0.0003); I² = 88%

Test for overall effect: Z = 2.19 (P = 0.03)

Mean

14.9

23.5

15.17

SD

2.4

7.3

4.83

Total

35

16

42

93

Mean

20.4

25.4

20.12

SD

2.5

5.9

5.87

Total

23

15

33

71

Weight

32.7%

32.2%

35.1%

100.0%

IV, Random, 95% CI

-2.22 [-2.90, -1.55]

-0.28 [-0.99, 0.43]

-0.92 [-1.40, -0.44]

-1.14 [-2.16, -0.12]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4

Favours yoga Favours control

PERCEIVED STRESS

Study

Chandwani et al., 2010

Danhauer et al., 2009

, 2011

Moadel et al., 2010

Raghavendra et al., 2007

Vadiraja et al., 2009

Total (95% CI)

Heterogeneity: Chi² = 40.64, df = 5 (P < 0.00001); I² = 88%

Test for overall effect: Z = 2.65 (P = 0.008)

Mean

5.9

14

7.06

17.16

16.6

12.91

SD

1.6

3.9

2.35

16.57

10.1

10.39

Total

27

13

16

84

28

47

215

Mean

5.4

19.9

16.69

21.88

29.9

21.85

SD

1.7

9.8

3.84

18.85

11.2

10.86

Total

31

14

16

44

34

44

183

Weight

17.5%

15.3%

13.0%

18.6%

17.3%

18.2%

100.0%

IV, Random, 95% CI

0.30 [-0.22, 0.82]

-0.76 [-1.54, 0.03]

-2.95 [-3.99, -1.91]

-0.27 [-0.64, 0.10]

-1.23 [-1.77, -0.68]

-0.83 [-1.26, -0.41]

-0.86 [-1.50, -0.22]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours yoga Favours control

DISTRESS

LONG-TERM EFFECTS

Study

Bower et al., 2011

Chandwani et al., 2010

Total (95% CI)

Heterogeneity: Chi² = 1.04, df = 1 (P = 0.31); I² = 4%

Test for overall effect: Z = 1.64 (P = 0.10)

Mean

9.9

7.7

SD

8

2.3

Total

16

27

43

Mean

10.5

9

SD

7.9

2.5

Total

15

29

44

Weight

37.0%

63.0%

100.0%

IV, Random, 95% CI

-0.07 [-0.78, 0.63]

-0.53 [-1.07, 0.00]

-0.36 [-0.80, 0.07]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-2 -1 0 1 2

Favours yoga Favours control

DEPRESSION

Study

Bower et al., 2011

, 2011

Total (95% CI)

Heterogeneity:Chi² = 24.36, df = 1 (P < 0.00001); I² = 96%

Test for overall effect: Z = 1.04 (P = 0.30)

Mean

23.6

16.94

SD

6.7

4.33

Total

16

16

32

Mean

24.2

32.69

SD

4.7

4.47

Total

15

16

31

Weight

50.9%

49.1%

100.0%

IV, Random, 95% CI

-0.10 [-0.81, 0.60]

-3.49 [-4.63, -2.34]

-1.76 [-5.08, 1.56]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours yoga Favours control

PERCEIVED STRESS

Study

Bower et al., 2011

Chandwani et al., 2010

, 2011

Total (95% CI)

Heterogeneity: Chi² = 46.83, df = 2 (P < 0.00001); I² = 96%

Test for overall effect: Z = 1.48 (P = 0.14)

Mean

23.6

4.9

1.69

SD

6.7

1.5

1.49

Total

16

27

16

59

Mean

24.2

4.5

18.19

SD

4.7

1.5

3.51

Total

15

29

16

60

Weight

34.8%

35.3%

30.0%

100.0%

IV, Random, 95% CI

-0.10 [-0.81, 0.60]

0.26 [-0.26, 0.79]

-5.97 [-7.67, -4.26]

-1.73 [-4.02, 0.56]

Yoga Control Std. Mean Difference Std. Mean Difference

IV, Random, 95% CI

-4 -2 0 2 4Favours yoga Favours control

DISTRESS

Figure 3 Effect sizes of yoga versus controls on psychological health: anxiety, depression, perceived stress, and psychological distress.

Cramer et al. BMC Cancer 2012, 12:412 Page 10 of 13http://www.biomedcentral.com/1471-2407/12/412

Table 4 Effect sizes of yoga versus no treatment and active control interventions

Outcomea No. ofstudies

No. ofpatients(yoga)

No. ofpatients(control)

Standardizedmean difference

[95% confidence interval]

P (overalleffect)

Heterogeneity

I2; Chi2; P

Yoga versus no treatment

Short-term

Global quality of life 3 127 85 0.29 [0.01, 0.57] 0.04 0%; 0.75; 0.69

Mental well-being 5 161 123 0.09 [−0.15, 0.33] 0.46 0%; 3.40; 0.49

Physical well-being 5 161 123 0.51 [−0.33, 1.34] 0.23 89%; 37.26; <0.01

Functional well-being 4 134 92 0.30 [0.03, 0.57] 0.03 0%; 1.14; 0.77

Social well-being 3 161 123 0.32 [0.08, 0.56] <0.01 0%; 3.49; 0.48

Spiritual well-being 2 97 58 0.41 [0.08, 0.74] 0.01 0%; 0.11; 0.74

Anxiety 2 111 75 −0.58 [−1.22, 0.07] 0.08 75%; 3.93; 0.05

Depression 2 40 45 −0.35 [−0.81, 0.12] 0.14 11%; 1.12; 0.29

Psychological distress 3 124 89 −0.19 [−0.70, 0.32] 0.47 64%; 5.55; 0.06

Yoga versus active control interventions

Short-term

Mental well-being 2 63 60 1.19 [0.13, 2.26] 0.03 81%; 5.9; 0.02

Anxiety 3 105 90 −2.21 [−3.90, -0.52] 0.01 95%; 42.26; <0.01

Depression 4 121 105 −2.29 [−3.97, -0.61] <0.01 96%; 74.01; <0.01

Perceived stress 3 93 71 −1.14 [−2.16, -0.12] 0.03 88%; 16.42; <0.01

Psychological distress 3 91 94 −1.55 [−2.48, -0.61] <0.01 85%; 13.68; <0.01aOutcomes are only shown when sufficient data for meta-analysis were available.

Table 5 Effect sizes of yoga versus control during active cancer treatment and after completion of active cancertreatment

Outcomea No. ofstudies

No. ofpatients(yoga)

No. ofpatients(control)

Standardized meandifference [95%

confidence interval]

P (overalleffect)

Heterogeneity

I2; Chi2; P

During active cancer treatment

Short-term

Mental well-being 3 90 91 1.01 [−0.19, 2.22] 0.10 92%; 24.89; <0.01

Physical well-being 3 81 82 1.22 [−0.90, 3.34] 0.26 97%; 28.66; <0.01

Social well-being 2 74 75 0.38 [−0.02, 0.78] 0.06 31%; 1.46; 0.23

Anxiety 4 132 121 −1.86 [−3.02, -0.69] <0.01 93%; 45.00;<0.01

Depression 4 132 121 −2.16 [−3.77, -0.55] <0.01 96%; 83.03; <0.01

Perceived stress 3 93 72 −2.13 [−3.48, -0.78] <0.01 91%; 21.38; <0.01

Psychological distress 4 113 114 −1.10 [−2.09, -0.10] 0.03 92%; 35.97; <0.01

After active cancer treatment

Short-term

Mental well-being 2 37 34 −0.16 [−0.63, 0.31] 0.50 0%; 0.04; 0.85

Physical well-being 2 37 34 0.07 [−0.68, 0.81] 0.86 44%; 1.77; 0.18

Functional well-being 2 37 34 0.23 [−0.23, 0.70] 0.33 0%; 0.05; 0.82

Social well-being 2 37 34 0.05 [−0.50, 0.61] 0.85 16%; 1.20; 0.27aOutcomes are only shown when sufficient data for meta-analysis were available.

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Cramer et al. BMC Cancer 2012, 12:412 Page 12 of 13http://www.biomedcentral.com/1471-2407/12/412

on breast cancer survivors [23,31]. This might have lim-ited the power of these analyses. Moreover, the respect-ive studies did not require participants to haveimpairments of health-related quality of life or psycho-logical health to be eligible, hence, leaving little room forimprovement.

External and internal validityThe included studies were conducted in primary, sec-ondary, and tertiary care settings in North America,Europe, or Asia. Participants were mainly adult Caucasiansand Asians but other ethnicities were also included.Patients with stage 0 to IV breast cancer and patientsundergoing active cancer treatment as well as survivorswho had completed active treatment were included.Most studies included mainly well educated women withhigh socioeconomic status and resulting good access tohealth care. However, 1 study explicitly aimed to includean ethnically diverse sample of breast cancer patients froman underserved urban community. The results of this re-view are therefore applicable to the vast majority ofbreast cancer patients and survivors in clinical practice.There was a great variability of risk of bias in included

studies. Blinding participants or care providers mightnot be possible in yoga studies [43]. However, blindingof outcome assessment is even more important andonly 3 studies reported blinding of outcome assessors[26,27,30]. Randomization and/or allocation concealmentwere inadequate in 50% of the included studies and theeffects on health-related quality of life were not distin-guishable from selection bias. These issues might limitinternal validity of the results regarding quality of life.In subgroup analyses, effects on psychological health

were only present in studies on patients undergoing ac-tive cancer treatment. Therefore, the results of this re-view are only applicable to breast cancer patients whoare undergoing active treatment.

Strengths and weaknessesThis is the first available systematic review and meta-analysis on yoga for breast cancer patients and survivors.Moreover, effects were analyzed separately for patients indifferent phases of active cancer treatment. Since adequaterandomization and allocation concealment have beenrecommended as the most important safeguard againstbias [44], effects of risk of selection bias were assessed.The primary limitation of this review is the small total

number of eligible RCTs. As only studies that were pub-lished as a full paper were eligible, this review mighthave missed RCTs that were unpublished or publishedas dissertation or abstract only. Moreover, as only 3RCTs included a long-term follow-up, long-term effectscould not be estimated for all pre-specified outcomemeasures and analyses were limited by the low number

of included studies. Interpretability of results is limitedby high risk of selection bias and detection bias. Hetero-geneity of yoga interventions regarding yoga tradition,length of the program and frequency of the interventionmight further limit the interpretation of the results. Atthe moment, it is impossible to make claims on whetherthe yoga style or other characteristics of the interventionhave any impact on the efficacy of the program. Statis-tical heterogeneity was high in most meta-analysis; 10out of 14 comparisons showed considerable heterogen-eity. Due to the low number of included studies, sub-group and sensitivity analyses could not provide reasonsfor heterogeneity in the remaining meta-analyses.

ConclusionsGiven the short period of time yoga has been regarded asa treatment option for breast cancer patients [45], the evi-dence reviewed here has to be regarded as preliminary.Some large studies on yoga for breast cancer patients arecurrently conducted by major US cancer centers [46] thatwill surely add new and possibly conflicting evidence.Until then, the clearly positive effects of yoga on psycho-logical health in breast cancer patients should warrant itsuse in this patient population. Yoga might be particularlyrecommended as an intervention to improve psychologicalhealth during active breast cancer treatment.

Competing interestsAll authors declare that they have no competing interests.

Authors’ contributionsHC was responsible for conception and design of the review, carried out theliterature search, performed data extraction and data analysis, and draftedthe manuscript. SL and PK performed data extraction and assessment of riskof bias, participated in conception and design of the review, and criticallyrevised the manuscript. AP and GD participated in conception and design ofthe review, and critically revised the manuscript. All authors read andapproved the final manuscript.

AcknowledgmentsThis review was supported by a grant from the Rut- andKlaus-Bahlsen-Foundation.

Received: 9 March 2012 Accepted: 12 September 2012Published: 18 September 2012

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doi:10.1186/1471-2407-12-412Cite this article as: Cramer et al.: Yoga for breast cancer patients andsurvivors: a systematic review and meta-analysis. BMC Cancer 201212:412.