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The effect of complementary and alternative medicine on the quality of life of cancer survivors: A systematic review and meta-analyses
Complementary Therapies in Medicine, 4, 21, pages 417 - 429
To assess whether quality of life (QOL) improved in cancer survivors who had undertaken a complementary and alternative medicine (CAM) intervention, compared to cancer survivors who had not.
A systematic review of randomised controlled trials (RCTs) was undertaken. Electronic databases including MEDLINE, Cochrane CENTRAL, CINAHL, PSYCHINFO, EMBASE, and ClinicalTrials.gov were searched from 1990 to 2012. Search terms incorporating the concepts of cancer survivors, QOL and various types of CAM were used.
From 1767 records retrieved and screened 13 full text articles were included in the review. Nine studies were deemed to have a high risk, one a low risk, and three an unclear risk of bias. CAM interventions used incorporated yoga, meditation or mindfulness, energy healing, medical qigong, homoeopathy, or mistletoe therapy. Ten of the studies used breast cancer survivors, whilst the remaining three included other cancer types. The studies had mixed results either showing a significantly greater improvement in QOL in the intervention group compared to the control group, or no significant difference between groups. However, twelve studies were of low to moderate quality, limiting the robustness of findings.
This review has identified significant gaps in the evidence base for the effectiveness of CAM on QOL in cancer survivors.
Further work in this field needs to adopt more rigorous methodology to help support cancer survivors to actively embrace self-management and effective CAMs, without recommending inappropriate interventions which are of no proven benefit.
Keywords: Cancer survivors, Quality of life, Complementary medicine, Alternative medicine.
Breakthroughs in cancer treatments and technologies mean that cancer patients are living longer, with over 64% surviving for at least five years after their initial cancer diagnosis.1 As a result of these advances a growing ageing cancer population has emerged.1
Cancer survivors are more likely to suffer from secondary health problems such as fatigue, anxiety, depression, nausea, and pain, as well as being at an increased risk of developing secondary tumours.2, 3, and 4 Many patients report feeling abandoned and isolated following cessation of active treatment,5 which could exacerbate symptoms such as depression and anxiety. This may have an impact on their quality of life (QOL), which has been reported as being lower than other population groups.6
It is important therefore to look at ways of improving cancer survivors’ QOL and long term health outcomes. QOL can be difficult to compare across different studies due to the multitude of scales that have been designed to evaluate it. However, in recent years more rigorous QOL tools have been developed, and the importance of recognising its value is reflected by the increasing number of studies specifying QOL as an outcome measure.7
Complementary and alternative medicine (CAM) has been defined as ‘a variety of different medical systems and therapies based on the knowledge, skills and practices derived from theories, philosophies and experiences used to maintain and improve health, as well as to prevent, diagnose, relieve or treat physical and mental illnesses. CAM has been mainly used outside conventional health care, but in some countries certain treatments are being adopted or adapted by conventional health care.’8 It encompasses a wide range of therapies including acupuncture, homoeopathy, meditation, chiropody, reflexology, and massage therapy.3 It has often been utilised by cancer patients as a way of regaining control over their bodies, developing therapeutic relationships with care providers, alleviating side-effects from treatment, and improving QOL. Having a strong belief in CAM, seeing CAM as a last resort, and finding hope from using CAM therapies have also been cited as reasons for uptake.2, 9, and 10 Previous studies have suggested that cancer patients have a higher use of CAM than the normal population.6, 11, and 12 It is estimated that across Europe 36% of cancer patients use some form of CAM,13 and a recent systematic review examining the number of cancer patients using CAM across North America, Australasia, and Europe found the combined prevalence across studies to be even higher at 40%.14
Despite this, little work has focused on the effect of CAM on QOL in cancer survivors, with the majority of systematic reviews examining its effect on people still under curative treatment.15, 16, 17, 18, 19, 20, 21, 22, 23, and 24 The aim of this systematic review was therefore to assess whether and what type of CAM improves QOL in cancer survivors.
Criteria for considering studies for this review
Types of studies
All randomised controlled trials (RCTs), quasi-RCTs and controlled before and after studies were considered for inclusion in this review. Observational cohort studies in which voluntary CAM users were compared with CAM non-users were excluded.
Types of participants
The population was limited to adults ≥18 years of age, with a previous cancer diagnosis who had finished their cancer treatment when the intervention was initiated, and were not undergoing palliative or terminal supportive care. The review aimed to include all types of cancer diagnosis. If ≥50% of study participants had completed their cancer treatment at the start of the intervention, the study was deemed eligible for inclusion.
Types of interventions
This review included studies where any type of CAM was used in the intervention group with QOL measured using a validated instrument, and including a control group without any CAM interventions. For the purpose of this review an intervention was classified as being CAM if it met the category criteria outlined by the US National Centre for Alternative and Complementary Medicine (NCCAM). These categories are natural products, mind and body medicine, manipulative and body based practices, movement therapies, traditional healers, energy fields, and whole medical systems.28
All studies were required to report QOL as a primary or secondary outcome measure to be eligible for inclusion.
The primary outcome for this review was changes in QOL in cancer survivors who had undertaken a CAM intervention, compared to those who had not. This review focused on overall QOL and two of its major domains-physical and mental QOL. Among the studies reviewed, overall QOL is measured by both the European Organisation for Research and Treatment of Cancer (EORTC)29 and the FACT B and G (Functional Assessment of General Health-Breast or General),30 The physical and mental domains of QOL are covered by subscales of these questionnaires and additionally the Short Form 36 (SF-36).
The secondary outcome for this review was adverse events. An adverse event in this context referred to any harm caused to participants from the CAM intervention.
Search methods for identification of studies
A search of the following databases was initially carried out on 23/01/2012:
MEDLINE, CENTRAL, CINAHL, PSYCHINFO and EMBASE.
Search terms were combined as in the following:
(‘Cancer patients’ OR ‘cancer survivors’ OR ‘oncology patients’),
AND (‘quality of life’ OR ‘wellbeing’)
AND (‘CAM’ OR ‘complementary medicine’ OR ‘complementary therapies’ OR ‘alternative medicine’ OR ‘alternative therapies’ OR ‘acupuncture’ OR ‘yoga’ OR ‘homeopathy’ OR ‘herbal medicine’ OR ‘phytotherapy’ OR ‘meditation’ OR ‘mindfulness’ OR ‘vitamin supplements’).
Both text words and indexed terms (such as MeSH) were used and they were modified as necessary in each database. The ClinicalTrials.gov database was also searched using the above terms to identify any finished but not yet published trials, as well as any trials that were still ongoing.
The search was updated and expanded on 20/02/2013 with the use of additional terms to cover herbal medicines commonly used by cancer patients31:
(‘Medicinal plants’ OR ‘plant extracts’ OR ‘aloe’ OR ‘ayurvedic medicine’ or ‘traditional Chinese medicine’ or ‘black cohosh’ or ‘flower remedies’ OR ‘carctol’ OR ‘chaparral’ OR ‘echinacea’ OR essiac’ OR ‘green tea’ OR ‘St John's wort’ OR ‘mistletoe’).
Searches were limited to papers published from 1990 onwards due to the relatively new focus of CAM on QOL of cancer survivors making it unlikely that relevant articles would be found prior to this time period. Articles of all languages were considered.
Selection of studies
All studies identified were screened for inclusion based on the study selection criteria. All titles and abstracts of articles which clearly did not fulfil the eligibility criteria were excluded. Full text copies of the remaining articles were obtained, and those not meeting the eligibility criteria were discarded. Those that remained were included in the systematic review. To ensure rigour in the study selection process two reviewers (CS, TT) independently checked through all the records identified to minimise bias. Any papers not unanimously excluded or included were re-examined by both reviewers until a consensus was reached. Fig. 1 illustrates the study selection process.
Any unreported information on the study's eligibility was sought by contacting the study author. If no response was given, the article was excluded from the review.
Data extraction and assessment of risk of bias
Data from included studies was extracted independently, discussed and collated, by two reviewers (CS and TT, YFC, or NG) using a data extraction form. The quality of the studies was independently assessed by two reviewers (CS, TT) using the Cochrane Collaboration's Tool for Assessing Risk of Bias.32 Any disagreement between the reviewers about the criteria or level of bias was discussed until a mutual decision was reached. Where necessary the study authors were contacted to obtain more detailed information.
Authors of six studies were contacted to obtain data to determine their eligibility in the review and/or data required for meta-analyses. Four authors provided the information requested.33, 34, 35, 36, and 37 Two studies where the authors were unable to provide sufficient data were excluded.38 and 39 Missing statistics were calculated where possible from other available statistics, and where standard deviations of change values were not reported they were calculated using a published method for imputing standard deviation.40
Studies with sufficient data which were judged to be sufficiently similar were pooled within each type of CAM according to the aforementioned categories defined by NCCAM, using RevMan 5.0 software. A standardised mean difference was calculated using a random effects model given the different QOL scales used between studies and the diversity of patient population and interventions. Tests for homogeneity within CAM groups were carried out using Chi2 tests, and I2 statistic was also computed.
Due to the large differences in follow-up time between studies, data was analysed to reflect short-term (3 months) and longer-term results (≥6 months).
Characteristics of included studies
Thirteen studies met the inclusion criteria. Characteristics of these studies are shown in Table 1. In total 1228 cancer patients were included: All were RCTs, including one unpublished study. Participants in all of the studies had previously received anti-cancer treatment with surgery, chemotherapy and/or radiotherapy. Ten of the thirteen studies consisted of cancer patients with a prior diagnosis of breast cancer. The average age of participants ranged from 49.8 to 63.9 years. Five studies evaluated the impact of yoga on QOL, three evaluated mindfulness/meditation, one meditation and yoga, one homoeopathy, one energy healing, one medical qigong, and one mistletoe therapy. Eleven studies were carried out in North America, one in Australia, and one in Europe.
|Study||Cancer type||Study country||Gender (% female)||Number of patients- intervention (I):control (C)||Length of intervention||Tool used for QOL||Mean age of participants (years)|
|Breast||USA||100||9:9||Eight weeks||FACT-B: overall QOL||62.9|
|85% breast, 15% unknown.||Canada||95||20:18||Seven weeks||EORTC QLQ-C30: overall QOL not reported||50|
|Breast||USA||100||22:22||Ten weeks||FACT-B: overall QOL||55.8|
|Breast||USA||100||108:56||Twelve weeks||FACT-G: overall QOL||54.8|
|Breast||USA||100||32:31||Six months||FACT-G: overall QOL||60|
|Breast||USA||100||53 (I1):52 (I2):58 (C)*||Five months||FACT-B: overall QOL||49.8|
|Breast||USA||100||41:43||Six weeks||SF-36: MCS and PCS||57.5|
|Breast||USA||100||64:66||Two years||FACT-B: overall QOL||63.9|
|Meditation and yoga|
|Breast 70.6%, other cancers 29.4%||USA||100||53:24||Eight weeks||EORTC QLQ-30: overall QOL||57.0|
|Breast||USA||100||30 (I1):26 (I 2):27 (C)**||One year||SF-36, only subscale general health reported||55.6|
|Breast||USA||100||17:14||Four weeks||FACT-B: overall QOL||52.5|
|Breast 37.7%, other cancers 62.3%||Australia||57.5||79:83||Ten weeks||FACT-G: overall QOL||60|
|Breast 100%||Europe||100||171 Intervention and control not known||Four weeks||SF-36||Not reported|
* Intervention 1 was MBSR intervention; intervention 2 was a nutrition education programme.
** Intervention 1 was a placebo combination medicine and a verum single remedy; intervention 2 was a verum combination medicine and a placebo single remedy.
Risk of bias in included studies
Overall nine studies were deemed to have a high risk33, 36, 41, 42, 43, 44, 45, 46, and 47 and one a low risk of bias.37 Three studies had an unclear risk of bias due to insufficient information being provided.48, 49, and 50Table 2 provides a summary of the risk of bias assessment for the 13 studies. The proportion of information from studies at high or unclear risk of bias was deemed sufficient to affect interpretation of results.
Black boxes represent a high risk of bias, grey boxes represent an unclear risk of bias, and white boxes represent a low risk of bias.
Descriptions of interventions and controls
Of the five studies using yoga as their main intervention, three practised hatha style yoga,41, 44, and 49 one restorative yoga,42 and one Iyengar yoga,45 and all were taught by experienced yoga instructors. All interventions were compared with a waitlist control group, and lasted ≤12 weeks, apart from one six month intervention.44 Yoga sessions were practiced at least weekly across studies, lasting 1–1.5
Two studies practised Mindfulness Based Stress Reduction (MBSR) in their intervention group vs. a waitlist control group,36 and 47 whilst a third used transcendental meditation vs. a control group that received basic breast cancer literature.33 One study36 incorporated a second intervention group consisting of a nutrition education programme. All meditation techniques were taught by trained instructors, and additional home practice monitored through participant self-report was encouraged in two studies.33 and 47 The classes were either hospital based36 and 47 or occurred in a community transcendental meditation centre.33 Intervention length and timings varied, with one having seven sessions of 1–1.5
Yoga and meditation
One study43 evaluated an intervention which included meditation, yoga, mindful communication skills and mindful breast examination/awareness. The intervention was undertaken in a hospital by a physician formally trained in yoga and MBSR. Nine sessions spanned eight weeks and lasted 2–4
This study37 consisted of two homoeopathic intervention groups, one consisting of a placebo combination medicine and a verum single remedy, and the other a verum combination medicine and a placebo single remedy, as well as a placebo control group. The medications were distributed over one year and participants were asked to self-medicate daily. Compliance was evaluated through asking participants to return any unwanted medication at study visits.
This hospital based study50 compared an energy healing intervention with a mock-healing control group. Two hour long sessions over eight weeks were performed. Energy healing practitioners were used in the intervention group, whilst mock healing was undertaken by researchers who were taught specific hand placement techniques.
The study46 using a medical qigong intervention vs. usual care control group lasted ten weeks, and consisted of 20 sessions lasting 90
This unpublished study,48 identified through a Cochrane review, was based in a rehabilitation clinic and compared subcutaneously administered mistletoe therapy vs. placebo in breast cancer patients who had previously completed adjuvant treatment. Twice weekly treatments over four weeks, followed by a four week observation period, were undertaken.
Effectiveness of CAM interventions on QOL
Table 3 provides a narrative summary of the effects of the interventions across the studies. Overall QOL was reported in eleven studies, physical QOL in seven studies, and mental QOL in eight studies. Quantitative data, including results of meta-analyses, are shown in Figure 2, Figure 3, Figure 4, and Figure 5. Data were available for meta-analyses from only six of the 13 studies, including four of the yoga studies (overall, physical and mental QOL at 3 months) and two of the meditation/mindfulness studies (overall QOL at 6 months).
|Overall risk of bias||Overall QOL||Physical QOL||Mental QOL|
|High risk||N/A||Physical wellbeing subscale of FACT-B at eight weeks, no significant difference vs. control, mean difference −0.05, CI 95% −0.76 to 0.66||Emotional wellbeing subscale of FACT-B at eight weeks, no significant difference vs. control, mean difference −0.19, CI 95% −31.30 to 30.92|
|High risk||EORTC, significantly better than control at 7 weeks, F
||N/A||Emotional function domain of EORTC significantly better at 7 weeks than control, F
|High risk||FACT-B, at 10 weeks, no significant difference vs. control mean difference 12.60, 95% CI −1.77 to 26.07, p
||Physical subscale of FACT-B, no significant difference vs. control, mean difference 2.40, 95% CI −1.56 to 6.36, p
||Emotional subscale of FACT-B, significantly better at three months than control, mean difference 3.0, 95% CI 0.11–5.89|
|Unclear risk||(From post hoc subgroup analysis) FACT-G, no significant difference vs. control at 3 months, mean difference 8.70, 95% CI −1.74 to 19.14||Physical subscale of FACT-G, no significant difference vs. control at 3 months, mean difference 0.98, 95% CI −2.07 to 4.03||Emotional subscale FACT-G, no significant difference vs. control at three months, mean difference 2.24, 95% CI −0.36 to 4.84|
|High risk||FACT-G, no significant difference vs. control at six months, mean difference 1.40, 95% CI −5.22 to 8.02, p
||Physical subscale of FACT-G, no significant difference vs. control, mean difference 0.60, 95% CI −1.13 to 2.33, p
||Emotional subscale of FACT-G, no significant difference vs. control, mean difference 0.00, 95% CI −1.64 to 1.64, p
|High risk||FACT-B at 5 months, no significant difference vs. control, mean difference 3.0, 95% CI −2.56 to 8.56||N/A||N/A|
|High risk||N/A||SF-36 PCS at 6 weeks, intervention 50.3 vs. control 46.9, mean difference 3.40, 95% CI 1.41–5.39||SF-36 MCS, at 6 weeks, intervention 53.0 vs. 50.1, mean difference 2.90, 95% CI 0.15 to 9 to 5.65|
|High risk||FACT-B, at two years, significantly better than control, mean difference 3.62, 95% CI 0.68–6.56, p
||Physical wellbeing subscale FACT-B, at two years, no difference between intervention and control, mean difference −0.69, 95% CI −1.97 to 0.59.||Emotional wellbeing subscale FACT-B, at two years, significantly better vs. control, mean difference 1.05, 95% CI 0.05–2.05.|
|Yoga and meditation|
|High risk||EORTC at 8 weeks, intervention group significantly improved between baseline and follow up, p
|Low risk||General health subscale of SF-36 only reported. Significant increase at 1 year in both homoeopathy groups vs. control, p
|Unclear risk||FACT-B at four weeks, no significant difference vs. control over time mean difference 4.8, CI −9.27 to 18.87.||N/A||N/A|
|High risk||FACT-G at 10 weeks, significantly better vs. control, mean difference 8.99, 95% CI 7.51–10.47, p
||Physical wellbeing subscale FACT-G significantly better vs. control, mean difference 2.08, 95% CI 0.65– 3.51, p
||Emotional wellbeing subscale FACT-G significantly better vs. control, mean difference 1.55, 95% CI 0.46–2.64, p
|Unclear||SF-36 at 8 weeks, no difference vs. control in overall QOL. Numerical data were not reported.||N/A||N/A|
Of the five yoga studies four reported on overall QOL. The pooled estimate of three studies shows a statistically significant difference in favour of yoga interventions at 3 months and the results were consistent across studies (Fig. 2; standardised mean difference 0.51, 95% CI 0.18–0.84, I2
Of the three studies two reported on overall QOL.33 and 36 The pooled result shows a small but statistically significant improvements in overall QOL (Fig. 3; standardised mean difference 0.32, 95% CI 0.06–0.57, I2
Yoga and meditation
This study reported significant improvements in overall QOL in the intervention group between baseline and follow up. However no numerical data was reported on differences between the intervention and control groups.43
This study reported only on the general health subscale of the SF-36 finding a significant increase at one year in both homoeopathy intervention groups vs. control.37
A greater improvement in overall QOL in the intervention group vs. control was found in this study, though this did not reach statistical significance.50
This study found significant differences in the intervention group vs. control when measuring overall QOL, and both the physical and mental domains of QOL using the FACT-G scale.
This study only reported details of the general health subscale of the SF-36 and found no significant differences between the intervention and control group. No numerical results were provided.47
Adverse effects were mentioned in two studies, one in which there was a significant increase in headaches in the group receiving homoeopathic combination (p
Summary of principal findings
This review has examined the effects of CAM on QOL in cancer survivors who have ceased active cancer treatment. Although the findings suggest that a number of CAM interventions may improve QOL in cancer survivors, the credibility of the results was weakened by the moderate to high risk of bias for most studies. In addition, the number of studies included for each type of CAM intervention was small, thus it was not possible to assess or rule out publication bias and chance findings.
Our review differs from other published systematic reviews in this area as it has a broader scope in terms of the types of CAM. It also focuses purely on cancer survivors, whereas most other existing research has examined cancer patients still undergoing active cancer treatment or patients in the palliative or terminal phases of their disease.15, 19, 20, 21, and 52 Despite our broader coverage of CAM, we only found a relatively small number of studies that focus on cancer survivors. The finding highlights a significant gap in the evidence base for the effectiveness of CAM on QOL in cancer survivors.
Evidence for individual CAM
Yoga appears to improve overall and mental QOL, but not physical QOL according to our meta-analyses. Two recent reviews also covered the effects of yoga on QOL in cancer survivors.15 and 16 Both included studies in which patients were still receiving active treatments. Culos-Reed et al. covered four of the five RCTs included in our review, but did not carry out meta-analysis.18 Based on various definitions of clinical significance, they concluded that yoga interventions hold promise for improving cancer survivors’ well-being. By contrast, Cramer et al. stated there is evidence of efficacy for yoga only during active cancer treatment but not after completion of active treatments.21 However the finding was based on a subgroup analysis containing only two of the five studies identified in our review.
Whilst the pooled estimate from our meta-analyses suggested a magnitude of effect that is clinically significant for yoga interventions,53 the results are based on studies of unclear or high risk of bias due to uncertainty in methods of randomisation, allocation concealment and blinding. The difficulty in blinding participants highlights a common challenge in separating out the true ‘intervention effect’ from a general ‘trial effect’ for many types of CAM. For example, the positive effect of yoga may come from the regular social interaction during the attendance of sessions rather than yoga itself. Future studies might benefit from incorporating a control group that features regular group sessions/social interactions to regulate the potential effects from these interactions.
Two published systematic reviews have examined mistletoe therapy.15 and 52 Again both included studies in which patients were receiving active cancer treatments. Kienle et al. reviewed controlled clinical studies and found that the majority reported a QOL benefit for mistletoe therapy.52 They included 10 RCTs in which mistletoe therapy was independent (i.e. not concomitant) of conventional cancer treatment. However seven of these studies were conducted by a single centre and measured only ‘self-regulation’ rather than general QOL, and none used a generic QOL tool. They were therefore not eligible for inclusion in our review. The majority of studies included in the Cochrane review on mistletoe therapy by Horneber et al. focused on patients who were receiving active cancer treatment or palliative care. Only one unpublished RCT, which found no significant differences between intervention and control groups, met our inclusion criteria. The quantity and quality of evidence is currently inadequate for an appropriate assessment of effectiveness for other types of CAM.
Limitations of this review
Every effort was made to provide a comprehensive and systematic review of the literature. However, it is possible that some studies may not have been captured in the search and screening process due the diversity of CAM and the difficulties in ascertaining whether cancer patients were still undergoing treatment. In addition, some of the information required for the review was not documented in the study papers, and contact with the study authors proved unfruitful.
The limited evidence identified in this review does not allow a comparison between different types of CAM. Nor are we able to explore whether the effects of a CAM vary between survivors of different types of cancer, with different prior treatments or at different stages of survivorship. These questions need to be addressed with further research.
The majority of included studies only recruited breast cancer patients. Although breast cancer is the most prevalent UK cancer today,54 it cannot be assumed that the results directly apply to other cancer survivors. Breast cancer patients may hold more positive outlooks, demonstrate fewer treatment effects, and have a higher QOL than patients with poorer prognoses. Breast cancer survivors are almost all female, and may hold different values towards CAM compared to males.
This review has identified significant gaps in the evidence base for the effectiveness of CAM on QOL in cancer survivors.
Further work in this field needs to adopt more rigorous methodology to help support cancer survivors to actively embrace self-management and effective CAMs, without recommending inappropriate interventions which are of no proven benefit.
Conflict of interest
No conflict of interest declared.
Role of the funding source
Study funded by the National Institute for Health Research. The study sponsors had no involvement in the study design, collection, analysis or interpretation of data, the writing of the manuscript or the decision to submit the manuscript for publication.
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University of Birmingham, Room 121, Primary Care Clinical Sciences, Edgbaston Campus, University of Birmingham, Birmingham B15 2TT, United Kingdom University of Birmingham, Room 121, Primary Care Clinical Sciences, Edgbaston Campus, University of Birmingham, Birmingham, B15 2TT, United Kingdom
Corresponding author at: Room 121/122, Primary Care Clinical Sciences, School of Health and Population Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom. Tel.: +44 0121 414 5483; fax: +44 0121 414 6571.
☆ Study funded by the National Institute for Health Research.
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