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Review

The impact of mindfulness-based interventions on symptom burden, positive psychological outcomes, and biomarkers in cancer patients

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Pages 121-131 | Published online: 01 Jun 2015

Abstract

Research on the use of mindfulness-based stress reduction and related mindfulness-based interventions (MBIs) in cancer care has proliferated over the past decade. MBIs have aimed to facilitate physical and emotional adjustment to life with cancer through the cultivation and practice of mindfulness (ie, purposeful, nonjudgmental, moment-to-moment awareness). This descriptive review highlights three categories of outcomes that have been evaluated in MBI research with cancer patients – namely, symptom reduction, positive psychological growth, and biological outcomes. We also examine the clinical relevance of each targeted outcome, while describing recently published original studies to highlight novel applications of MBIs tailored to individuals with cancer. Accumulating evidence suggests that participation in a MBI contributes to reductions in psychological distress, sleep disturbance, and fatigue, and promotes personal growth in areas such as quality of life and spirituality. MBIs may also influence markers of immune function, hypothalamic–pituitary–adrenal axis regulation, and autonomic nervous system activity, though it remains unclear whether these biological changes translate to clinically important health benefits. We conclude by discussing methodological limitations of the extant literature, and implications of matching MBIs to the needs and preferences of cancer patients. Overall, the growing popularity of MBIs in cancer care must be balanced against scientific evidence for their impact on specific clinical outcomes.

Introduction

Cancer is a leading cause of mortality worldwide, with 1.7 million new diagnoses and 585,720 deaths estimated during 2014 in the United States alone.Citation1,Citation2 Diagnosis, treatment, and survivorship are associated with a complex array of stressors including treatment side effects; changes in daily activities; disrupted social, family, and occupational roles; and the possibility of cancer recurrence and death.Citation3Citation5 To buffer the effects of these and other stressors, the use of integrative mind–body therapies for cancer care is common. Recent data suggest that 32% of cancer survivors report current or past use of mind–body interventions such as meditation, yoga, and stress management to promote emotional and physical well-being and to reduce psychological distress.Citation6,Citation7

One type of mind–body intervention that has been well studied in cancer populations is mindfulness-based stress reduction (MBSR), a program designed to assist individuals in coping with physical and/or emotional challenges through the cultivation and practice of mindfulness.Citation8 The program is semimanualized, meaning that sessions are structured and follow general principles, but they also allow the interventionist to flexibly adapt session content based on participant needs and concerns. Mindfulness is a concept rooted in ancient Buddhist tradition that refers to purposeful, nonjudgmental, moment-to-moment awareness.Citation9 This is in contrast to the experience of automatically reacting to experience, ruminating about the past, and worrying about the future, which may be prominent in individuals facing a life-threatening diagnosis such as cancer.Citation10 The ability to engage in mindful awareness is associated with improved psychological distress and physical health symptoms in populations with chronic illness, including cancer.Citation11,Citation12

MBSR was first developed by Kabat-Zinn et al in the late 1970s to help relieve suffering among individuals with chronic pain, anxiety, and other unexplained medical symptomatology.Citation8,Citation13 The traditional MBSR program involves eight weekly 150-minute sessions consisting of didactic instruction, group discussion, formal meditation practice (eg, body scan, sitting meditation, walking meditation, loving kindness), gentle hatha yoga, plus a 6-hour silent meditation retreat.Citation8 Essential components also include regular home-based mindfulness meditation and the incorporation of mindfulness into everyday activities. This framework serves as the basis for various MBSR adaptations with various formats and durations, collectively called mindfulness-based interventions (MBIs), that have been used with cancer patients. Two formalized MBIs that have been evaluated in oncology populations include mindfulness-based cognitive therapy (MBCT),Citation21,Citation22 which combines the MBSR curriculum with principles of cognitive therapy and was originally intended for the treatment of depression, and mindfulness-based cancer recovery (MBCR),Citation10 one of the most widely evaluated cancer-specific adaptations of MBSR that involves eight 90-minute group classes with content tailored to the unique stressors and experiences associated with cancer. We refer to programs as MBIs if they were developed from Kabat-Zinn’s original MBSR framework and if they do not involve only meditation or yoga.

The literature on MBIs for patients with cancer has been synthesized elsewhere several times between 2005 and 2015 in meta-analyses,Citation23Citation29 literature reviews,Citation12,Citation30Citation34 and book chapters.Citation35Citation37 The aim of this paper is to add to this literature by providing a nonsystematic, descriptive review of MBI outcomes that have been empirically evaluated in cancer populations, with a focus on recently published original studies to highlight research trends and novel applications. The process used to retrieve studies involved an initial search for review papers on MBIs for cancer patients using search terms such as “mindfulness”, “mindfulness-based interventions”, “mindfulness-based stress reduction”, “mindfulness-based cancer recovery”, “mindfulness-based cognitive therapy”, “cancer”, and/or “oncology” in PubMed, PsycINFO, and Google Scholar, followed by a search within reference lists for additional review papers. We then completed an additional search for original studies published since 2014 that had not been included in review articles. Readers are encouraged to consult existing review papers and original articles for more systematic details of methods, samples, and outcomes that have been evaluated in MBI studies.

We outline three categories of outcomes that have been most widely studied – symptom reduction, positive psychological outcomes, and biomarkers – and describe why each outcome might represent a suitable target of intervention in cancer care. Understanding the range of benefits individuals might experience following MBI participation will help ensure interventions are consistent with a particular patient’s goals, values, and clinical characteristics, which could impact adherence and outcomes.Citation38Citation41 This review could serve as a springboard for future investigations into the following questions: which desired outcomes can be targeted by MBIs? And for whom might MBIs be well-suited?

Symptom reduction

Individuals with cancer are prone to multiple symptoms associated with the disease, its treatment, and comorbid conditions. Symptoms may include psychological distress, sleep disturbance, shortness of breath, nausea, diarrhea, pain, lymphedema, vasomotor symptoms, and anemia.Citation38,Citation42 MBIs may play an important role in helping patients manage mental and physical health symptoms, and in reducing the impact of cancer-related symptoms on overall functioning and quality of life.Citation42,Citation43 The most widely evaluated symptoms in MBI studies with cancer patients include psychological distress, sleep disturbance, and fatigue, so these are outlined below. It is noteworthy that preliminary evidence exists for the use of MBIs to reduce other cancer symptoms such as pain, sexual difficulties, and hot flashesCitation20,Citation44Citation46 and that MBIs have been widely used to alleviate some of these symptoms (especially pain) in noncancer populations.Citation12,Citation47,Citation48

Psychological distress

Individuals living with cancer commonly experience psychological distress throughout the illness trajectory.Citation49,Citation50 Psychological distress is a multidimensional concept that exists along a continuum, and is most commonly assessed using measures of affective states, symptoms of stress, anxiety, and depressed mood.Citation12,Citation51,Citation52 It is estimated that 30%–43% of cancer patients exceed clinical cutoffs for psychological distress on self-report instruments.Citation52 Up to 38% meet diagnostic criteria for major depression and 18% meet criteria for an anxiety disorder, though estimates vary depending on the measurement method and cancer type.Citation49,Citation53 Psychological distress can interfere with the ability to cope with cancer and, while still very controversial, some research suggests that persistent high levels of distress may adversely impact cancer progression and survival.Citation51,Citation54,Citation55

Psychological distress also represents the most frequently evaluated outcome in clinical studies of MBIs with cancer populations.Citation12,Citation31 To our knowledge, six meta-analyses have been published to date that examine the association of MBI participation with measures of psychological distress in people living with cancer.Citation23Citation26,Citation28,Citation29 Most recently, Zainal et alCitation28 examined nine studies,Citation15,Citation56Citation61,Citation85,Citation101 including two randomized controlled trials (RCTs),Citation15,Citation61 that investigated 6- to 8-week MBIs among women with breast cancer. The results indicate medium to large pooled effects on symptoms of stress, depression, and anxiety. Medium to large effects are also reported in prior meta-analyses of MBIs among cancer patients for improvements in depressed mood and anxiety,Citation23,Citation26,Citation29 perceived stress and mood disturbance,Citation29 distress,Citation25 as well as aggregated mental health outcomes (ie, anxiety, depressed mood, stress, and psychological components of quality of life).Citation24 A recent RCT of the traditional MBSR program among 336 women with stage I–III breast cancer indicated that medium to large improvements in depressed mood and anxiety, relative to usual care, were maintained at the 12-month follow-up.Citation62 Further, there is growing evidence that MBIs are superior to active control conditions on some measures of distress, including depressed mood, anxiety, and stress symptoms.Citation61,Citation63

Narrative reviews and clinical practice guidelines suggest that there is strong evidence for the use of MBIs to improve symptoms of stress, anxiety, and depression among individuals coping with cancer.Citation12,Citation38 However, most original studies have utilized uncontrolled, pre-post designs; have primarily recruited early-stage, nonmetastatic breast cancer patients; and have measured affective symptoms using self-report rather than formal diagnostic procedures. In addition, heightened baseline distress is not consistently used as an inclusion criterion in MBI studies. It therefore remains unclear whether MBIs are appropriate for the treatment of anxiety and/or mood disorders in cancer patients, whether some results would be more pronounced if participants were screened for distress or, in pre–post studies, whether reductions in distress are attributable to the intervention. To date, no MBI studies have selectively recruited cancer patients with diagnosed depression or anxiety; however, there is evidence from pre–post studies in noncancer populations that MBIs are associated with large effects on anxious and depressive symptoms in patients with psychological disorders.Citation64 Since 2014, there has been ongoing work to remedy some of these limitations by examining the use of MBIs to reduce distress in oncology samples with diagnoses other than breast cancer,Citation14,Citation17,Citation65Citation68 relatively greater severity of illness,Citation68,Citation69 other phases of illness including end of life and survivorship,Citation20,Citation68 and with measurement of distress using randomized designs and comparison groups.Citation20,Citation65,Citation66,Citation70

Sleep disturbance

Sleep is a significant problem for many cancer patients. Prevalence estimates suggest that the risk of insomnia symptoms is increased two- to three-fold in cancer patients, and that symptoms persist for years following cancer treatment in up to 44% of patients.Citation71,Citation72 Sleep disturbances such as insomnia can be caused or worsened by treatment side effects, pain, and psychological distress that are common in cancer, and they can be maintained by maladaptive sleep behaviors, dysfunctional cognitions about sleep, and physiological arousal.Citation71,Citation73 Despite the common co-occurrence of insomnia with psychological distress, including anxiety and depression,Citation74 insomnia symptoms represent a distinct clinical entity that may warrant its own focus in psychosocial interventions.Citation75

To capitalize upon potential benefits of mindfulness for alleviating disturbed sleep, a number of RCTs have tested the impact of MBIs on sleep parameters in oncology populations, including four published in 2014 alone.Citation14,Citation16,Citation20,Citation70,Citation76Citation79 Some of these studies report associations between MBIs and improvements in self-reported insomnia severity,Citation14,Citation70 sleep quality,Citation20,Citation78 sleep onset latency and wake time after sleep onset,Citation70 sleep difficulties/disturbance,Citation16,Citation79 and in actigraphic measures of sleep quality/quantity,Citation70,Citation77 with some changes observed 12 weeks following program completion.Citation77 Associations between MBIs and improvements in sleep have not always been significant relative to active treatment and waitlist comparison groups,Citation70,Citation76,Citation77,Citation79 and some findings may not be significant after correction for potential type I error.Citation16,Citation77 It is possible that more robust results would be observed if patients were selected for pre-existing sleep difficulty, given that most trials have not involved the a priori decision to target sleep, but rather included sleep-related measures as ancillary outcomes of larger RCTs.Citation14,Citation16,Citation20,Citation76Citation78

A notable exception is the recent study by Garland et al,Citation70 in which all patients were required to meet research and diagnostic criteria for insomnia. This study reported the results from a RCT comparing MBCR to cognitive–behavioral therapy for insomnia among 111 patients with various cancer diagnoses. This trial was unique in that patients chose to participate in order to address insomnia rather than to learn meditation skills; they were also blinded to the treatment options at study consent, and they were informed only about their own assigned intervention. A noninferiority analysis indicated post-treatment insomnia symptoms were less severe in participants who completed cognitive–behavioral therapy relative to those who completed MBCR; however, MBCR was noninferior to cognitive–behavioral therapy for improving insomnia severity at the 3-month follow-up, with both groups showing subthreshold insomnia symptoms. These findings suggest that while MBCR may be slower to take effect on disturbed sleep relative to cognitive–behavioral therapy, both treatments produce clinically significant improvements in sleep in the longer term.

In general, it appears that MBIs may represent a treatment option for cancer patients with sleep difficulties, and that the effect of MBIs on sleep can be significant in light of the chronicity of insomnia in many individuals (eg, a mean of 7 years insomnia duration in Garland et alCitation70). Although there are currently no evidence-based guidelines on the use of MBIs for improving sleep in cancer patients, presumably due to insufficient evidence to date, it is encouraging to see renewed interest in the use of MBIs for cancer-related sleep difficulties since the first sleep outcomes of a 6-week MBSR program in cancer patients were published in 2003.Citation76 Additional, well-designed, adequately powered controlled trials are needed to further establish the effect of MBIs in patients with insomnia who seek out this form of treatment.

Fatigue

Another frequently investigated cancer symptom in MBI research has been cancer-related fatigue (CRF), a persistent pattern of tiredness and diminished energy that is inconsistent with changes in sleep or activity levels and interferes with day-to-day functioning.Citation80,Citation81 CRF is one of the most common and distressing symptoms of cancer, with prevalence estimates suggesting that 59%–100% of cancer patients experience fatigue, and that 9%–56% experience clinically significant CRF.Citation42,Citation82,Citation83 For up to 40% of patients, problems with fatigue persist for months or years following cancer treatment.Citation84

Among studies that have evaluated fatigue as an outcome of MBIs in cancer populations,Citation20,Citation58,Citation69,Citation85Citation88 two RCTs that have specifically targeted fatigue as a primary outcome deserve mention.Citation14,Citation89 Johns et alCitation14 examined an abbreviated MBI for reducing fatigue among 35 post-treatment cancer survivors with CRF. The intervention consisted of seven 2-hour classes that involved education about CRF, training and practice in mindfulness meditation, and gentle hatha yoga, as well as 20 minutes of daily home practice. Relative to a waitlist group, patients who completed the MBI reported lower fatigue severity, lower fatigue interference, and greater vitality postprogram and at 1-month follow-up. The results corresponded to large effects and persisted after correction for multiple comparisons and statistical adjustment for baseline fatigue, mindfulness skills, and participation in recent mental health treatment. It is also noteworthy that all participants were retained from baseline through to 1-month follow-up, intervention attendance was high (88%), and the interventionist was blind to patient outcomes. Similarly, van der Lee and GarssenCitation89 randomized 100 post-treatment cancer patients with significant fatigue to either a waitlist control or to an eight-session program, modified from the original MBCT program described earlier,Citation22 to include psychoeducation about CRF in the place of depression content and an added exercise on coping with interpersonal boundaries. Following adjustment for baseline fatigue, fatigue severity was lower in MBCT participants relative to controls, which corresponded to a large effect that was maintained at the 6-month follow-up.

These findings support the possibility of tailoring MBIs to alleviate CRF, and they are consistent with the conclusions of review articles suggesting that MBIs are likely to be effective in the treatment of CRF,Citation81 and that there is moderate evidence for the use of MBIs to alleviate CRF.Citation90 However, MBIs for fatigue also need to be investigated among patients with more severe cancer, given that a recent nonrandomized feasibility study involving a small group of 19 women with metastatic breast cancer indicated that standard 8-week MBSR was not associated with reductions in CRF from baseline to 4 months postprogram.Citation69 Future work is also needed to confirm the utility of fatigue-specific MBIs with larger samples and to examine potential biobehavioral mechanisms through which mindfulness might influence CRF.

Positive psychological outcomes

There is growing recognition that the prominent focus on pathological outcomes in psychosocial oncology overlooks potential experiences of personal growth and meaning-making that can arise from the cancer experience,Citation43,Citation91 which may serve as an important buffer to psychological distress.Citation43 Similarly, it has been suggested that psychosocial interventions in cancer populations should target and evaluate not just symptom reduction, but also positive psychological outcomes that may arise.Citation13,Citation43,Citation91

The most frequently evaluated positive psychosocial outcome in MBI research has been quality of life – that is, “individuals’ perception of their position in life in the context of the culture and value systems in which they live and in relation to their goals, expectations, standards, and concerns”.Citation92 Musial et alCitation25 reported on four single-arm studies and two RCTs representing 248 cancer patients with mixed diagnoses who had received some form of MBI.Citation16,Citation58,Citation86,Citation93Citation95 Overall, there was a small effect of these MBIs on postprogram quality of life. Improvements in self-reported general well-being were also observed 1 year following an 8-week MBI that included cognitive therapy elements in 47 patients with mixed cancer diagnoses.Citation86 Consistent with these findings, clinical practice guidelines indicate that there is strong evidence that meditation practice, including formal MBI participation, is associated with improved quality of life in patients treated for breast cancer.Citation38

In addition to improvements in quality of life, several single-group studies and RCTs with cancer patients have demonstrated that MBIs are associated with positive changes in other areas such as spirituality, positive affect, meaningfulness, acceptance, comfort, happiness, relaxation, and post-traumatic growth.Citation20,Citation46,Citation61,Citation96 However, positive psychological outcomes of MBIs have not consistently been superior to usual care or active comparison groups.Citation15,Citation96 Pooled results from two RCTs with oncology populations indicate no significant group differences between MBIs and usual care in terms of spiritual well-being outcomes (ie, the quality of life dimension that involves a sense of purpose, peace of mind, and finding comfort in one’s spiritual beliefs).Citation15,Citation23,Citation61,Citation97 In one of these two studies, though, breast cancer patients in 8-week standard MBSR did show significantly greater improvements in spirituality when compared to both usual care and a nutrition education condition, which were maintained relative to the active control at the 12-month follow-up.Citation61

As an example of a recent study that has evaluated positive psychological outcomes from MBIs, Thornton et alCitation17 evaluated a 20-session intervention that incorporated MBSR with sessions focused on values-based goal setting, stress management, social support, assertive communication, sexuality, and health behaviors. Thirty-two women with recurrent breast or gynecological cancer received the intervention over a 7-month period. There were medium to large improvements from baseline to postprogram in terms of hope, mindfulness, positive affect, and quality of life. Interestingly, greater mindfulness and hope were related to lower mood disturbance, anxiety, and depressive symptoms, suggesting that positive psychological outcomes tend to co-occur with reductions in psychological distress.

Qualitative studies also help generate a subjective understanding of positive psychological benefits that cancer patients might experience from mindfulness training. Responses in interviews, focus groups, and open-ended questionnaires with oncology samples who completed mindfulness training (either on its own or as part of a structured MBI) reveal themes of spirituality, personal growth, optimism, peacefulness, confidence, acceptance, openness, connectedness, happiness, general satisfaction, and appreciation of the group process and shared experience.Citation68,Citation69,Citation98Citation102 For example, Visser et alCitation99 interviewed nine women with advanced breast cancer about their experiences during a group-based MBI that involved eight weekly 2.5-hour sessions and a 1-day silent retreat. Themes revealed in the qualitative interviews suggest that patients felt that mindfulness training led them to have greater awareness of their thoughts and feelings, increased acceptance of their health condition, improved energy, better communication with significant others, and social support from other participants.Citation99 Similarly, van den Hurk et alCitation68 interviewed six patients with lung cancer and five partners of lung cancer patients who had participated in a MBSR program that included psychoeducation about grief. Participants reported that mindfulness practice had initiated a positive process of change, characterized by experiences such as standing still (eg, relaxing, taking time for themselves), being aware, insight into thoughts and feelings, letting go, changing behavior, and acceptance. Existing quantitative and qualitative findings suggest that patients may achieve a number of positive psychological benefits as a result of MBI participation, although future research is needed to clarify inconsistent findings.

Biomarkers

In addition to lessening some of the symptoms associated with cancer and promoting personal growth, evidence is beginning to emerge that MBI participation is associated with alterations in potentially important biological markers of stress and health.Citation12,Citation55,Citation103 Biomarkers that have been shown to change following participation by cancer patients in MBIs include measures of immune function,Citation20,Citation94,Citation95,Citation104,Citation105 hypothalamic–pituitary–adrenal axis regulation,Citation63,Citation94,Citation104Citation107 prostate-specific antigen levels,Citation108 and autonomic nervous system activity;Citation46,Citation94,Citation109 not all biological changes, however, were observed relative to control groups. Literature reviews have generally concluded that MBIs show small but significant effects on biomarkers and physical health.Citation24,Citation29 Matchim et alCitation29 reviewed four studies of MBIs in cancer patients and reported a small significant effect on biological outcomes in most studies,Citation94,Citation95,Citation105,Citation106 with the exception of a large effect of MBCR on cytokine production at 6- and 12-month follow-up in an uncontrolled study with breast and prostate cancer patients.Citation94 Similarly, a review of eight studies reported that MBIs show a small effect on physical health parameters including biomarkers (eg, levels of cortisol and interleukin 6, natural killer cell activity) and physical symptoms (eg, self-reported gastrointestinal and neurologic issues) in cancer populations.Citation24

Since the publication of these literature reviews, two RCTs have investigated the impact of MBSRCitation110 and MBCRCitation111 on additional biomarkers – namely, telomere length and telomerase activity – in breast cancer patients. Telomeres are specialized structures that protect chromosome ends, with shorter telomere length associated with cellular aging, whereas telomerase is a ribonucleoprotein enzyme involved in telomere maintenance and elongation.Citation112 Both studies report promising results, such that telomere length was maintained following MBCR relative to a minimal intervention control condition,Citation111 and telomerase activity improved more in MBSR relative to usual care and was sustained at 12-week follow-up.Citation110 These two studies add to the growing literature on the potential effects of MBIs on biomarkers of health, given that shorter telomere length and telomerase activity have been shown to predict cancer mortality.Citation113Citation115

Taken together, these findings suggest that various biological parameters may serve as subtle but significant markers of treatment response to MBIs, and they may represent mechanisms through which psychosocial function could impact physical health.Citation55,Citation116 However, it will be crucial in future research to ensure that immune–endocrine outcomes are straightforward to interpret and have relevance for health.Citation117 For instance, whether enhanced natural killer cell function is desirable or not may depend on the type and stage of cancer, the phase of treatment, and the baseline level of this biomarker of immune system activity. Further, biomarker response to MBIs may differ as a function of patient sex, cancer type, and baseline biologic values.Citation106,Citation107,Citation109 The causal pathways linking MBIs to both stress reduction and biological activity are also unclear, such that biological changes can be a cause and/or effect of behavioral comorbidities such as psychological distress, depressed mood, fatigue, and impaired sleep.Citation103 Therefore, the relationship between biomarker response to MBIs and long-term health or cancer symptoms is not well understood.

Discussion and implications

MBIs have become increasingly popular programs to assist cancer patients as they navigate the experience of living with the disease. It is clear that the mindfulness approach is a versatile one, with an abundance of benefits that may arise from realizing that one can “slow down and see things as they are, without blinders, and learn ways to hold the strong emotions and sensations that arise”.Citation12 In returning to the initial question of which desired outcomes can be targeted by MBIs, the most consistently demonstrated benefit in cancer and noncancer populations is reduced psychological distress (perhaps, in part, because it is also the most routinely assessed outcome).Citation12,Citation118 Additional benefits may include reductions in sleep disturbance and fatigue, as well as improvements in overall quality of life, positive well-being, and spirituality. There is also growing evidence that MBIs may influence biological parameters, though it remains to be seen whether or not the changes observed translate into clinically significant health benefits for the patient.

A commonly reported reason for the use of MBIs and other complementary therapies by cancer patients is to promote general self-care and wellness, though some patients also desire specific outcomes such as enhanced immune function and reduced pain, distress, and insomnia.Citation6,Citation119 This suggests the importance of using existing empirical data on patient outcomes to ensure MBIs are matched to patient needs and preferences. For example, an individual seeking improvements in distress, sleep, fatigue, and/or positive psychological well-being may be satisfied with the program given the demonstrated ability of MBIs to influence these outcomes. In contrast, it is less clear whether MBIs can influence other symptoms a patient might hope to alleviate, such as pain, sexual issues, nausea, or cognitive dysfunction.Citation38 It is also possible that MBI retention could be improved if relevant content is added to interventions that target specific symptoms. Among patients joining a MBI to treat insomnia, for example, it may be important to provide education about insomnia and evidence supporting the use of mindfulness practice for disturbed sleep. Additional research is needed to assess whether the addition of symptom-specific modules can favorably influence MBI uptake, adherence, and outcomes.

Though some patients may join MBIs with the hope of improving biological outcomes,Citation6 it is currently premature to conclude that these interventions can influence variables such as immune function or cellular aging in clinically meaningful ways. Research on biomarker outcomes has shown small effects, inconsistent findings, and has yet to demonstrate links to health outcomes such as cancer progression and longevity. Therefore, it is important to ensure prospective MBI participants have realistic expectations about the biological outcomes they might achieve, while still appreciating that research on biomarkers may contribute to our understanding about mechanisms of action and treatment response.Citation107,Citation110,Citation120,Citation121 It will be interesting for future studies to continue examining how biomarkers relate to changes in mindfulness and psychosocial outcomes, including symptom reduction and positive well-being.

In terms of general research limitations, high attrition from MBIs, lack of long-term follow-up, and non-RCT designs continue to be methodological issues in some studies.Citation24,Citation33 The majority of research on MBIs also involves relatively small samples of self-selecting, educated, middle-aged White women with breast cancer, which could limit generalizability to individuals with different symptoms, prognoses (eg, those in the palliative stage of cancer), sociodemographics (eg, males), and views about mindfulness.Citation27,Citation28,Citation33 Although participation in MBIs may assist cancer patients in dealing with symptoms of distress, sleep disturbance, or fatigue, it is currently not clear whether these interventions are useful to those living with other symptoms. As well, since these types of interventions only appeal to a subset of patients, the utility of the broad application of MBIs to all cancer patients and survivors is unknown. In addition, variability across studies in terms of outcome measures, cancer stage, and intervention content makes it difficult to compare findings or evaluate the “active ingredients” of MBIs.Citation25 Some authors have indicated a need for greater investigation of how MBIs compare to other efficacious interventions (eg, cognitive–behavioral therapy), and how various “doses” of MBI (eg, program duration, amount of daily mindfulness practice) compare in their ability to improve outcomes.Citation12,Citation34,Citation70,Citation122

Recent and ongoing research shows promise in some of these areas. For example, Kenne Sarenmalm et alCitation123 plan to perform a 5-year follow-up in a RCT of MBSR for psychological distress in breast cancer patients, which will provide relatively long-term data on MBI outcomes. Also, van den Hurk et alCitation68 published a mixed methods pilot study on MBSR for lung cancer patients (53% men) and their partners, demonstrating the feasibility of delivering MBIs within a nonbreast cancer sample. There has also been methodological progress with respect to abbreviated and online versions of MBIs designed to reduce the burden of program participation,Citation14,Citation48,Citation65,Citation123 and the inclusion of partners or close significant others in MBIs.Citation68,Citation104,Citation124,Citation125 For example, Wood et alCitation125 recently published a session-by-session protocol for adapting MBCT to the caregivers of cancer patients. Partner involvement could be of added value considering that partners commonly report psychological distress that is inter-related with patient distress, and that there is preliminary evidence for the idea that partner participation in MBIs can reduce caregiver burden.Citation68,Citation126,Citation127

Overall, the growing popularity of MBSR and other MBIs for cancer patients must be balanced against scientific evidence for their impact on specific clinical outcomes.Citation122 With the potential appeal of mindfulness training as a panacea to promote all facets of health and well-being, clinicians must be aware of the current state of evidence for the use of MBIs to facilitate physical and emotional adjustment to cancer.

Acknowledgments

Dr Linda E Carlson holds the Enbridge Research Chair in Psychosocial Oncology at the University of Calgary Cumming School of Medicine, cofunded by the Canadian Cancer Society Alberta/Northwest Territories Division and Alberta Cancer Foundation. Dr Sheila N Garland is a postdoctoral fellow funded by a Canadian Institutes for Health Research (CIHR) Bisby Fellowship. Codie R Rouleau is funded by a CIHR Doctoral Award and an Alberta Innovates Health Solutions (AIHS) Graduate Studentship.

Disclosure

The authors report no conflicts of interest in this work.

References

  • StewartBWWildCPWorld Cancer Report 2014Lyon, FranceInternational Agency for Research on Cancer2014
  • American Cancer SocietyCancer Facts and Figures 2014Atlanta, GAAmerican Cancer Society2014 Available from: http://www.cancer.org/acs/groups/content/@research/documents/webcontent/acspc-042151.pdfAccessed May 3, 2015
  • FallowfieldLJenkinsVPsychosocial/survivorship issues in breast cancer: are we doing better?J Natl Cancer Inst2015107133525432407
  • HewittMBreenNDevesaSCancer prevalence and survivorship issues: analyses of the 1992 National Health Interview SurveyJ Natl Cancer Inst199991171480148610469749
  • AlfanoCMRowlandJHRecovery issues in cancer survivorship: a new challenge for supportive careCancer J200612543244317034679
  • MaoJJPalmerCSHealyKEDesaiKAmsterdamJComplementary and alternative medicine use among cancer survivors: a population-based studyJ Cancer Surviv20115181720924711
  • DengGCassilethBComplementary or alternative medicine in cancer care-myths and realitiesNat Rev Clin Oncol2013101165666423897081
  • Kabat-ZinnJFull Catastrophe Living: Using the Wisdom of Your Body and Mind to Face Stress, Pain, and IllnessNew York, NYDelacourt1990
  • BishopSRLauMShapiroSMindfulness: a proposed operational definitionClinical Psychology: Science and Practice200411230241
  • CarlsonLESpecaMMindfulness-Based Cancer RecoveryOakland, CANew Harbinger2010
  • DobkinPLZhaoQIncreased mindfulness – the active component of the mindfulness-based stress reduction program?Complement Ther Clin Pract2011171222721168110
  • CarlsonLEMindfulness-based interventions for physical conditions: a narrative review evaluating levels of evidenceISRN Psychiatry2012201265158323762768
  • ShapiroSLCarlsonLEThe Art and Science of Mindfulness: Integrating Mindfulness into Psychology and the Helping ProfessionsWashington, DCAmerican Psychological Association Publications2009
  • JohnsSABrownLFBeck-CoonKMonahanPOTongYKroenkeKRandomized controlled pilot study of mindfulness-based stress reduction for persistently fatigued cancer survivorsPsychooncology Epub8172014
  • LengacherCAJohnson-MallardVPost-WhiteJRandomized controlled trial of mindfulness-based stress reduction (MBSR) for survivors of breast cancerPsychooncology200918121261127219235193
  • MontiDAPetersonCKunkelEJA randomized, controlled trial of mindfulness-based art therapy (MBAT) for women with cancerPsychooncology200615536337316288447
  • ThorntonLMCheavensJSHeitzmannCADorfmanCSWuSMAndersenBLTest of mindfulness and hope components in a psychological intervention for women with cancer recurrenceJ Consult Clin Psychol20148261087110024884347
  • HendersonVPMassionAOClemowLHurleyTGDrukerSHébertJRA randomized controlled trial of mindfulness-based stress reduction for women with early-stage breast cancer receiving radiotherapyIntegr Cancer Ther201312540441323362338
  • BartleyTMindfulness-Based Cognitive Therapy for CancerWest Sussex, UKWiley-Blackwell2012
  • BowerJECrosswellADStantonALMindfulness meditation for younger breast cancer survivors: A randomized controlled trialCancer201512181231124025537522
  • SegalZVWilliamsJMTeasdaleJDMindfulness-Based Cognitive Therapy for DepressionNew York, NYThe Guilford Press2002
  • SegalZWilliamsMTeasdaleJMindfulness-Based Cognitive Therapy for Depression: A New Approach to Preventing Relapse1st edNew York, NYThe Guilford Press2001
  • CramerHLaucheRPaulADobosGMindfulness-based stress reduction for breast cancer-a systematic review and meta-analysisCurr Oncol2012195e343e35223144582
  • LedesmaDKumanoHMindfulness-based stress reduction and cancer: a meta-analysisPsychooncology200918657157919023879
  • MusialFBüssingAHeusserPChoiKEOstermannTMindfulness- based stress reduction for integrative cancer care: a summary of evidenceForsch Komplementmed201118419220221934319
  • PietJWürtzenHZachariaeRThe effect of mindfulness-based therapy on symptoms of anxiety and depression in adult cancer patients and survivors: a systematic review and meta-analysisJ Consult Clin Psychol20128061007102022563637
  • ShneersonCTaskilaTGaleNGreenfieldSChenYFThe effect of complementary and alternative medicine on the quality of life of cancer survivors: a systematic review and meta-analysesComplement Ther Med201321441742923876573
  • ZainalNZBoothSHuppertFAThe efficacy of mindfulness-based stress reduction on mental health of breast cancer patients: a meta-analysisPsychooncology20132271457146522961994
  • MatchimYArmerJMStewartBRMindfulness-based stress reduction among breast cancer survivors: a literature review and discussionOncol Nurs Forum2011382E61E7121356643
  • MackenzieMJCarlsonLESpecaMMindfulness-based stress reduction (MBSR) in oncology: rationale and reviewEvidence-Based Integrative Medicine200523139145
  • MatchimYArmerJMMeasuring the psychological impact of mindfulness meditation on health among patients with cancer: a literature reviewOncol Nurs Forum20073451059106617878133
  • OttMJNorrisRLBauer-WuSMMindfulness meditation for oncology patients: a discussion and critical reviewIntegr Cancer Ther2006529810816685074
  • ShennanCPayneSFenlonDWhat is the evidence for the use of mindfulness-based interventions in cancer care? A reviewPsychooncology201120768169720690112
  • SmithJERichardsonJHoffmanCPilkingtonKMindfulness-based stress reduction as supportive therapy in cancer care: systematic reviewJ Adv Nurs200552331532716194185
  • CarlsonLEMeditation and physical healthWestMAThe Psychology of Meditation: Research and Practice2nd edOxford, UKOxford University PressIn Press
  • CarlsonLEMindfulness meditation and yoga for cancer patientsHollandJCBreitbartWSJacobsenPBLoscalzoMJMcCorkleRButowPNPsycho-Oncology3rd edOxford, UKOxford University Press2015492
  • ShapiroSCarlsonLMindfulness-based interventions for physical healthThe Art and Science of Mindfulness: Integrating Mindfulness into Psychology and the Helping ProfessionsWashington, DCAmerican Psychological Association Publications20097591
  • GreenleeHBalneavesLGCarlsonLESociety for Integrative Oncology Guidelines Working GroupClinical practice guidelines on the use of integrative therapies as supportive care in patients treated for breast cancerJ Natl Cancer Inst Monogr201420145034635825749602
  • KemperKBullaSKruegerDOttMJMcCoolJAGardinerPNurses’ experiences, expectations, and preferences for mind-body practices to reduce stressBMC Complement Altern Med2011112621481259
  • WürtzenHDaltonSOAndersenKKWho participates in a randomized trial of mindfulness-based stress reduction (MBSR) after breast cancer? A study of factors associated with enrollment among Danish breast cancer patientsPsychooncology20132251180118522592966
  • CarlsonLETamagawaRStephenJTailoring mind-body therapies to individual needs: patients’ program preference and psychological traits as moderators of the effects of mindfulness-based cancer recovery and supportive-expressive therapy in distressed breast cancer survivorsJ Natl Cancer Inst Monogr201420145030831425749597
  • Esther KimJEDoddMJAouizeratBEJahanTMiaskowskiCA review of the prevalence and impact of multiple symptoms in oncology patientsJ Pain Symptom Manage200937471573619019626
  • ShapiroSLLopezAMSchwartzGEQuality of life and breast cancer: relationship to psychosocial variablesJ Clin Psychol200157450151911255204
  • BrottoLAHeimanJRGoffBA psychoeducational intervention for sexual dysfunction in women with gynecologic cancerArch Sex Behav200837231732917680353
  • BrottoLAHeimanJRMindfulness in sex therapy: applications for women with sexual difficulties following gynecologic cancerSex Relation Ther2007221311
  • Bauer-WuSSullivanAMRosenbaumEFacing the challenges of hematopoietic stem cell transplantation with mindfulness meditation: a pilot studyIntegr Cancer Ther200872626918550888
  • ChiesaASerrettiAMindfulness-based interventions for chronic pain: a systematic review of the evidenceJ Altern Complement Med2011171839321265650
  • DowdHHoganMJMcGuireBEComparison of an online mindfulness-based cognitive therapy intervention with online pain management psychoeducation: a randomized controlled studyClin J Pain Epub162015
  • MassieMJPrevalence of depression in patients with cancerJ Natl Cancer Inst Monogr200432577115263042
  • ZaboraJRBlanchardCGSmithEDPrevalence of psychological distress among cancer patients across the disease continuumJournal of Psychosocial Oncology19971527387
  • National Comprehensive Cancer Network, IncPractice Guidelines in Oncology – v.1.2002: Distress Management. Version 1Jentintown, PANational Comprehensive Cancer Network, Inc2002
  • ZaboraJBrintzenhofeSzocKCurbowBHookerCPiantadosiSThe prevalence of psychological distress by cancer sitePsychooncology2001101192811180574
  • StarkDKielyMSmithAVelikovaGHouseASelbyPAnxiety disorders in cancer patients: their nature, associations, and relation to quality of lifeJ Clin Oncol200220143137314812118028
  • BrownKWLevyARRosbergerZEdgarLPsychological distress and cancer survival: a follow-up 10 years after diagnosisPsychosom Med200365463664312883115
  • LutgendorfSKSoodAKBiobehavioral factors and cancer progression: physiological pathways and mechanismsPsychosom Med201173972473022021459
  • MatousekRHPruessnerJCDobkinPLChanges in the cortisol awakening response (CAR) following participation in mindfulness-based stress reduction in women who completed treatment for breast cancerComplement Ther Clin Pract2011172657021457893
  • MatousekRHDobkinPLWeathering storms: a cohort study of how participation in a mindfulness-based stress reduction program benefits women after breast cancer treatmentCurr Oncol2010174627020697517
  • LengacherCAJohnson-MallardVBartaMFeasibility of a mindfulness-based stress reduction program for early-stage breast cancer survivorsJ Holist Nurs201129210711721041554
  • TacónAMCalderaYMRonaghanCMindfulness-based stress reduction in women with breast cancerFamilies, Systems, and Health2004222193203
  • TacónAMMindfulness effects on symptoms of distress in women with cancerJournal of Cancer Pain and Symptom Palliation2006221722
  • HendersonVPClemowLMassionAOHurleyTGDrukerSHébertJRThe effects of mindfulness-based stress reduction on psychosocial outcomes and quality of life in early-stage breast cancer patients: a randomized trialBreast Cancer Res Treat201213119910921901389
  • WürtzenHDaltonSOElsassPMindfulness significantly reduces self-reported levels of anxiety and depression: results of a randomised controlled trial among 336 Danish women treated for stage I-III breast cancerEur J Cancer20134961365137323265707
  • CarlsonLEDollRStephenJRandomized controlled trial of mindfulness-based cancer recovery versus supportive expressive group therapy for distressed survivors of breast cancerJ Clin Oncol201331253119312623918953
  • HofmannSGSawyerATWittAAOhDThe effect of mindfulness-based therapy on anxiety and depression: A meta-analytic reviewJ Consult Clin Psychol201078216918320350028
  • ZernickeKACampbellTSSpecaMMcCabe-RuffKFlowersSCarlsonLEA randomized wait-list controlled trial of feasibility and efficacy of an online mindfulness-based cancer recovery program: the eTherapy for cancer applying mindfulness trialPsychosom Med201476425726724804884
  • StaffordLThomasNFoleyEComparison of the acceptability and benefits of two mindfulness-based interventions in women with breast or gynecologic cancer: a pilot studySupport Care Cancer20152341063107125281227
  • SchellekensMPvan den HurkDGPrinsJBStudy protocol of a randomized controlled trial comparing mindfulness-based stress reduction with treatment as usual in reducing psychological distress in patients with lung cancer and their partners: the MILON studyBMC Cancer201414324386906
  • van den HurkDGSchellekensMPMolemaJSpeckensAEvan der DriftMAMindfulness-based stress reduction for lung cancer patients and their partners: results of a mixed methods pilot studyPalliat Med Epub2202015
  • EylesCLeydonGMHoffmanCJMindfulness for the self-management of fatigue, anxiety, and depression in women with metastatic breast cancer: a mixed methods feasibility studyIntegr Cancer Ther2015141425625161198
  • GarlandSNCarlsonLEStephensAJAntleMCSamuelsCCampbellTSMindfulness-based stress reduction compared with cognitive behavioral therapy for the treatment of insomnia comorbid with cancer: a randomized, partially blinded, noninferiority trialJ Clin Oncol201432544945724395850
  • SavardJSavardMHInsomnia and cancer: prevalence, nature, and nonpharmacologic treatmentSleep Med Clin201383373387
  • SavardJMorinCMInsomnia in the context of cancer: a review of a neglected problemJ Clin Oncol200119389590811157043
  • HarveyAGA cognitive model of insomniaBehav Res Ther200240886989312186352
  • American Psychiatric AssociationDiagnostic and Statistical Manual of Mental Disorders5th edArlington, VAAmerican Psychiatric Publishing2013
  • BuysseDJAngstJGammaAAjdacicVEichDRösslerWPrevalence, course, and comorbidity of insomnia and depression in young adultsSleep200831447348018457234
  • ShapiroSLBootzinRRFigueredoAJLopezAMSchwartzGEThe efficacy of mindfulness-based stress reduction in the treatment of sleep disturbance in women with breast cancer: an exploratory studyJ Psychosom Res2003541859112505559
  • LengacherCAReichRRPatersonCLThe effects of mindfulness-based stress reduction on objective and subjective sleep parameters in women with breast cancer: a randomized controlled trialPsychooncology201524442443224943918
  • AndersenSRWürtzenHSteding-JessenMEffect of mindfulness- based stress reduction on sleep quality: results of a randomized trial among Danish breast cancer patientsActa Oncol201352233634423282113
  • LipschitzDLKuhnRKinneyAYDonaldsonGWNakamuraYReduction in salivary α-amylase levels following a mind-body intervention in cancer survivors – an exploratory studyPsychoneuroendocrinology20133891521153123375640
  • PortenoyRKItriLMCancer-related fatigue: guidelines for evaluation and managementOncologist19994111010337366
  • MitchellSAHoffmanAJClarkJCPutting evidence into practice: an update of evidence-based interventions for cancer-related fatigue during and following treatmentClin J Oncol Nurs201418Suppl385825427608
  • DonovanKAMcGintyHLJacobsenPBA systematic review of research using the diagnostic criteria for cancer-related fatiguePsychooncology201322473774422544488
  • WeisJCancer-related fatigue: prevalence, assessment and treatment strategiesExpert Rev Pharmacoecon Outcomes Res201111444144621831025
  • ServaesPVerhagenSBleijenbergGDeterminants of chronic fatigue in disease-free breast cancer patients: a cross-sectional studyAnn Oncol200213458959812056710
  • MatchimYArmerJMStewartBREffects of mindfulness-based stress reduction (MBSR) on health among breast cancer survivorsWest J Nurs Res2011338996101620956583
  • Kieviet-StijnenAVisserAGarssenBHudigWMindfulness-based stress reduction training for oncology patients: patients’ appraisal and changes in well-beingPatient Educ Couns200872343644218657376
  • GarlandSNTamagawaRToddSCSpecaMCarlsonLEIncreased mindfulness is related to improved stress and mood following participation in a mindfulness-based stress reduction program in individuals with cancerIntegr Cancer Ther2013121314022505593
  • CarlsonLEGarlandSNImpact of mindfulness-based stress reduction (MBSR) on sleep, mood, stress and fatigue symptoms in cancer outpatientsInt J Behav Med200512427828516262547
  • van der LeeMLGarssenBMindfulness-based cognitive therapy reduces chronic cancer-related fatigue: a treatment studyPsychooncology201221326427222383268
  • PachmanDRPriceKACareyECNonpharmacologic approach to fatigue in patients with cancerCancer J201420531331825299140
  • Casellas-GrauAFontAVivesJPositive psychology interventions in breast cancer. A systematic reviewPsychooncology201423191923897834
  • World Health OrganizationProgramme on Mental Health: WHOQOL Measuring Quality of Life GenevaSwitzerlandWorld Health Organization1997
  • FoleyEBaillieAHuxterMPriceMSinclairEMindfulness-based cognitive therapy for individuals whose lives have been affected by cancer: a randomized controlled trialJ Consult Clin Psychol2010781727920099952
  • CarlsonLESpecaMFarisPPatelKDOne year pre-post intervention follow-up of psychological, immune, endocrine and blood pressure outcomes of mindfulness-based stress reduction (MBSR) in breast and prostate cancer outpatientsBrain Behav Immun20072181038104917521871
  • CarlsonLESpecaMPatelKDGoodeyEMindfulness-based stress reduction in relation to quality of life, mood, symptoms of stress, and immune parameters in breast and prostate cancer outpatientsPsychosom Med200365457158112883107
  • GarlandSNCarlsonLECookSLansdellLSpecaMA non- randomized comparison of mindfulness-based stress reduction and healing arts programs for facilitating post-traumatic growth and spirituality in cancer outpatientsSupport Care Cancer200715894996117611782
  • BredleJMSalsmanJMDebbSMArnoldBJCellaDSpiritual well-being as a component of health-related quality of life: the Functional Assessment of Chronic Illness Therapy – Spiritual Well-Being scaleReligions2011217794
  • ChadwickPNewellTSkinnerCMindfulness groups in palliative care: a pilot qualitative studySpirituality and Health International200893135144
  • VisserAde WitteTSpeckensAEPrinsJBvan LaarhovenHWA qualitative analysis of experiences of patients with metastatic breast cancer participating in a mindfulness-based interventionPalliat Med201529218218325160693
  • MackenzieMJCarlsonLEMunozMSpecaMA qualitative study of self-perceived effects of mindfulness-based stress reduction (MBSR) in a psychosocial oncology settingStress Health20072315969
  • DobkinPLMindfulness-based stress reduction: what processes are at work?Complement Ther Clin Pract200814181618243937
  • HoffmanCJErsserSJHopkinsonJBMindfulness-based stress reduction in breast cancer: a qualitative analysisComplement Ther Clin Pract201218422122623059436
  • MillerAHAncoli-IsraelSBowerJECapuronLIrwinMRNeuroendocrine-immune mechanisms of behavioral comorbidities in patients with cancerJ Clin Oncol200826697198218281672
  • LengacherCAKipKEBartaMA pilot study evaluating the effect of mindfulness-based stress reduction on psychological status, physical status, salivary cortisol, and interleukin-6 among advanced-stage cancer patients and their caregiversJ Holist Nurs201230317018522442202
  • Witek-JanusekLAlbuquerqueKChroniakKRChroniakCDurazo-ArvizuRMathewsHLEffect of mindfulness based stress reduction on immune function, quality of life and coping in women newly diagnosed with early stage breast cancerBrain Behav Immun200822696998118359186
  • CarlsonLESpecaMPatelKDGoodeyEMindfulness-based stress reduction in relation to quality of life, mood, symptoms of stress and levels of cortisol, dehydroepiandrosterone sulfate (DHEAS) and melatonin in breast and prostate cancer outpatientsPsychoneuroendocrinology200429444847414749092
  • BränströmRKvillemoPAkerstedtTEffects of mindfulness training on levels of cortisol in cancer patientsPsychosomatics201354215816423218058
  • SaxeGAHébertJRCarmodyJFCan diet in conjunction with stress reduction affect the rate of increase in prostate specific antigen after biochemical recurrence of prostate cancer?J Urol200116662202220711696736
  • CampbellTSLabelleLEBaconSLFarisPCarlsonLEImpact of Mindfulness-Based Stress Reduction (MBSR) on attention, rumination and resting blood pressure in women with cancer: a waitlist-controlled studyJ Behav Med201235326227121667281
  • LengacherCAReichRRKipKEInfluence of mindfulness-based stress reduction (MBSR) on telomerase activity in women with breast cancer (BC)Biol Res Nurs201416443844724486564
  • CarlsonLEBeattieTLGiese-DavisJMindfulness-based cancer recovery and supportive-expressive therapy maintain telomere length relative to controls in distressed breast cancer survivorsCancer2015121347648425367403
  • GreiderCWTelomere length regulationAnnu Rev Biochem1996653373658811183
  • RossiDLobetti BodoniCGenuardiETelomere length is an independent predictor of survival, treatment requirement and Richter’s syndrome transformation in chronic lymphocytic leukemiaLeukemia20092361062107219340005
  • GhaffariSHShayan-AslNJamialahmadiAHAlimoghaddamKGhavamzadehATelomerase activity and telomere length in patients with acute promyelocytic leukemia: indicative of proliferative activity, disease progression, and overall survivalAnn Oncol200819111927193418567608
  • WilleitPWilleitJMayrATelomere length and risk of incident cancer and cancer mortalityJAMA20103041697520606151
  • MatousekRHDobkinPLPruessnerJCortisol as a marker for improvement in mindfulness-based stress reductionComplement Ther Clin Pract2010161131920129404
  • MillerGECohenSPsychological interventions and the immune system: a meta-analytic review and critiqueHealth Psychol2001201476311199066
  • KhouryBLecomteTFortinGMindfulness-based therapy: a comprehensive meta-analysisClin Psychol Rev201333676377123796855
  • WeitzMVFisherKLachmanVDThe journey of women with breast cancer who engage in mindfulness-based stress reduction: a qualitative explorationHolist Nurs Pract2012261222922157506
  • LabelleLECampbellTSFarisPCarlsonLEMediators of mindfulness-based stress reduction (MBSR): assessing the timing and sequence of change in cancer patientsJ Clin Psychol2015711214025099479
  • OngJCUlmerCSManberRImproving sleep with mindfulness and acceptance: a metacognitive model of insomniaBehav Res Ther2012501165166022975073
  • BishopSRWhat do we really know about mindfulness-based stress reduction?Psychosom Med2002641718311818588
  • Kenne SarenmalmEMårtenssonLBHolmbergSBAnderssonBAOdénABerghIMindfulness based stress reduction study design of a longitudinal randomized controlled complementary intervention in women with breast cancerBMC Complement Altern Med20131324824088535
  • BirnieKGarlandSNCarlsonLEPsychological benefits for cancer patients and their partners participating in mindfulness-based stress reduction (MBSR)Psychooncology20101991004100919918956
  • WoodAWGonzalezJBardenSMMindful caring: using mindfulness-based cognitive therapy with caregivers of cancer survivorsJ Psychosoc Oncol2015331668425397963
  • MoserMTKünzlerANussbeckFBargetziMZnojHJHigher emotional distress in female partners of cancer patients: prevalence and patient-partner interdependencies in a 3-year cohortPsychooncology201322122693270123825026
  • HodgesLJHumphrisGMMacfarlaneGA meta-analytic investigation of the relationship between the psychological distress of cancer patients and their carersSoc Sci Med200560111215482862