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Mind–Body Therapies for Cancer Survivors: Effects of Yoga and Mindfulness Meditation on Cancer-Related Physical and Behavioral Symptoms 

Mind–Body Therapies for Cancer Survivors: Effects of Yoga and Mindfulness Meditation on Cancer-Related Physical and Behavioral Symptoms
Chapter:
Mind–Body Therapies for Cancer Survivors: Effects of Yoga and Mindfulness Meditation on Cancer-Related Physical and Behavioral Symptoms
Author(s):

Chloe C. Boyle

and Julienne E. Bower

DOI:
10.1093/med/9780199380862.003.0030
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Introduction

Cancer is primarily a disease of aging, and the majority of cancer diagnoses occur among individuals over 65 years of age. Fortunately, advances in cancer detection and treatment have resulted in longer survival times for individuals diagnosed with cancer. As a consequence, there are a growing number of cancer survivors in the United States, most of whom are older adults. Indeed, of the current 14.5 million cancer survivors in the United States, approximately 60% are 65 years and older, and nearly a quarter were diagnosed more than 15 years prior (DeSantis et al., 2014).

Older survivors typically demonstrate better psychological adjustment than younger survivors, perhaps because they have had experience confronting other major life stressors and health challenges. However, they are at risk for physical problems and limitations following cancer diagnosis and treatment (Reeve et al., 2009). These include declines in physical functioning as well as cancer-related fatigue, pain, and sleep disturbance (Bellury et al., 2011). Depression is also prevalent in cancer patients and survivors, including elderly cancer survivors (Mitchell et al., 2011). All of these symptoms have a negative impact on quality of life and may also predict shorter survival (Groenvold et al., 2007).

The management of physical and behavioral symptoms among older survivors is an important challenge for researchers and clinicians (Rowland & Bellizzi, 2014). Medications used to treat pain and sleep problems have unwanted side effects, and pharmacological approaches have shown limited efficacy in treating symptoms like cancer-related fatigue (Bower, 2014). Further, patients may be reluctant to take additional medications to manage the side effects of their cancer treatments (Naeim et al., 2014; Rao & Cohen, 2004). Mind–body therapies are purported to target a wide array of mental and physical ailments, and have shown efficacy in alleviating psychological distress among cancer survivors (e.g., Buffart et al., 2012; Ledesma & Kumano, 2009). Two of the most common mind–body therapies used in cancer populations are yoga and mindfulness meditation. Here, we consider the evidence that these therapies influence cancer-related physical and behavioral symptoms that are common among older cancer survivors, including physical and functional well-being, fatigue, sleep disturbance, pain, and depression. We first present a general overview of these symptoms, then review the results of randomized controlled trials (RCTs) assessing the efficacy of yoga and mindfulness-based interventions on these symptoms. As of yet, there is very little research on whether mind–body approaches are specifically helpful for older cancer survivors. Indeed, older adults remain consistently underrepresented in both research and intervention trials of all types (Rowland & Bellizzi, 2014). Thus, we consider all RCTs conducted with adult cancer survivors, regardless of age at diagnosis, that have examined effects on the symptoms of interest. To identify studies for inclusion, we searched MEDLINE, PsychInfo, and ISI through December 2014. Searches were limited to human studies and the English language. We searched using the following terms: “mindfulness,” “meditation,” “yoga,” “cancer,” and “randomized controlled trial.” We also screened the reference lists of selected reviews and primary articles for additional publications.

Overview of Cancer-Related Symptoms

Physical and Functional Well-Being

Physical and functional well-being may include mobility, muscle strength, stamina, the ability to perform activities of daily living, and the extent to which declines in physical health interfere with important life roles (Stein et al., 2008). Prospective studies indicate that older survivors report significantly worse physical functioning than cancer-free controls. These differences are small, but may persist for up to 10 years past diagnosis and beyond (Lazovich et al., 2009; Reeve et al., 2009; Stein et al., 2008). Difficulties with physical function may be amplified by comorbid medical conditions among older cancer survivors, the most common of which are diabetes, chronic obstructive pulmonary disease, and congestive heart failure (Edwards et al., 2014; Rowland & Bellizzi, 2014). As many as 40% of cancer survivors over the age of 65 have at least one comorbidity, and this number increases with age (Edwards et al., 2014).

Functional decline has reciprocal relations with other cancer-related symptoms. Patients who experience fatigue, pain, or depression may decrease their physical activity, placing them at greater risk for functional problems (Bellury et al., 2011). In turn, functional problems may interfere with participation in valued activities or may create dependency on others, leading to isolation, loneliness, and psychological distress (Stein et al., 2008).

Fatigue

Fatigue is one of the most common and distressing side effects of cancer and its treatment, and may endure for months or years after treatment completion (Bower, 2014). Indeed, up to one-third of cancer survivors report persistent post-treatment fatigue. Patient reports suggest that cancer-related fatigue is more severe, more persistent, and more debilitating than “normal” fatigue caused by lack of sleep or overexertion and is not relieved by adequate sleep or rest (Poulson, 2001). Cancer-related fatigue is multidimensional and may have physical, mental, and emotional manifestations, including generalized weakness, diminished concentration or attention, decreased motivation or interest to engage in usual activities, and emotional lability (Bower, 2014).

Younger survivors typically report higher levels of fatigue than older survivors (Champion et al., 2014). However, fatigue is still prevalent in older survivors and is associated with lower levels of physical activity and reduced muscle strength in this population (Winters-Stone et al., 2008). Thus, fatigue may be a risk factor for physical deconditioning and frailty in older patients. Comorbidities may also increase the risk for fatigue in older survivors.

Sleep

Sleep disturbance is common in cancer patients, including difficulty getting to sleep and maintaining sleep during the night (e.g., frequent awakenings, difficulty resuming sleep, waking early). Sleep disturbance may be present before, during, and after treatment (Irwin, 2013). In a recent population-based longitudinal study of 962 patients, over 50% reported insomnia symptoms after diagnosis, which persisted at 18 months post-diagnosis in 36% of survivors (Savard et al., 2011). Of note, 21% of survivors in this study met criteria for clinically significant insomnia, that is, sleep problems that are severe and persistent enough to cause impairments in daytime functioning. Similarly high prevalence estimates have been observed in longer-term survivors, including those over age 60, suggesting that sleep problems may be enduring without treatment (Bardwell & Profant, 2008; Savard et al., 2001).

Like fatigue, rates of insomnia tend to be higher in younger than older survivors (Irwin, 2013), but older survivors may still fare worse than age-matched controls with no cancer history. In one study of older lung cancer survivors an average of 8 years past treatment, 56.5% reported poor sleep quality, compared to 30% in controls (Gooneratne et al., 2007).

Pain

Pain is one of the most feared symptoms for cancer patients and survivors, and more than one-third of post-treatment survivors report moderate to severe pain (van den Beuken-van Everdingen et al., 2007). Longer-term survivors are also at risk, with 5%–10% reporting chronic pain severe enough to interfere with functioning (Glare et al., 2014). Chronic pain may arise from surgery, chemotherapy, or radiation therapy, and treatment combinations (which are frequent in modern cancer treatment) may increase the likelihood of pain (Glare et al., 2014). Up to 40% of postmenopausal breast cancer survivors report arthralgias, or joint pain and stiffness, following hormonal therapies such as aromatase inhibitors; this is particularly problematic given that current guidelines recommend that women take these medications for up to 10 years post-treatment (Glare et al., 2014).

The relationship between age and pain is not clear. Older age is a risk factor for chemotherapy-induced peripheral neuropathy, but in general, studies have found less, more, and equivalent levels of pain among younger and older cancer patients (Glare et al. 2014; van den Beuken-van Everdingen et al., 2007). Nociception does not appear to change with age, but older adults may report less pain, perhaps from an unwillingness to complain, lower expectations for pain control, or an assumption that pain is age related and normative (Rao & Cohen, 2004). Older adults are more vulnerable to increased toxicity from pharmacological approaches to pain treatment (Rao & Cohen, 2004).

Depression

Cancer survivors are at substantially increased risk for depression. While estimates of prevalence vary, approximately 20% of all cancer patients are likely to experience depression or significant depressive symptoms (Irwin, 2013; Mitchell et al., 2011). Rates of depression are highest at diagnosis and treatment and typically decline across the survivorship period (Mitchell et al., 2013). A recent meta-analysis found no relationship between age and depression among cancer survivors (Mitchell et al., 2011).

Despite its prevalence, depression likely remains underrecognized and undertreated, particularly among older cancer survivors (Weinberger et al., 2011). Assessing depression can be particularly difficult in older adults; presentation of symptoms may be subclinical or atypical, characterized by somatic complaints and anhedonia rather than sadness (Naeim et al., 2014). Even when detected, older cancer survivors may be less likely than younger survivors to be referred for psychological treatment by healthcare providers (Weinberger et al., 2011).

Summary

The literature on cancer-related physical and behavioral symptoms indicates that these symptoms are common among older cancer survivors and occur at higher rates than individuals with no cancer history. Importantly, these symptoms may persist for years after successful treatment, creating an enduring burden for otherwise healthy survivors and for those who are managing other health conditions. Thus, targeted interventions may be required to improve symptoms and to prevent declines in physical function. The possibility that yoga and mindfulness-based interventions may be helpful in alleviating cancer-related symptoms is considered in the following sections.

Yoga Interventions: Effects on Behavioral and Physical Symptoms in Cancer Survivors

Description of Interventions

We focus here on RCTs of yoga conducted with cancer survivors—that is, individuals who have completed primary cancer treatment with surgery, radiation, and/or chemotherapy. We have included studies with a primary focus on yoga that examined effects on physical function and/or behavioral symptoms, and we report on these outcomes in Table 30.1. Of note, because self-report measures are the gold standard for the assessment of subjective symptoms, we focused on these outcomes for the purposes of this review.

Table 30.1. Description of Randomized Controlled Yoga Interventions

Author, Year

Population

Time Post-Diagnosis or Treatment

Number of Participants (Yoga, Control), % Female

Age (Mean)

Intervention Type and Duration

Control Group

Assessments*

Outcomes**

Between Group Difference ***

Effect Size for Between Group Difference (Cohen’s D)

Banasik (2011)

Breast cancer survivors

At least 2 months post-treatment

18 (9Y, 9C), 100% female

Y: 62.4 yrs (SD = 7.3); C: 63.3 yrs (SD = 6.9)

  • Iyengar yoga, 8 weeks, 2×/week

  • Intervention described as an “active” practice, with physically demanding poses. Primarily focused on poses, no meditation.

Wait list

Baseline, post-intv

Physical well-being (FACT)

NS

NR

Functional well-being (FACT)

NS

NR

Fatigue

Y > C

NR

Bower (2012)

Breast cancer survivors with fatigue

Median = 1.7 yrs post-treatment (range = 0.7–18.3 yrs)

31 (16Y, 15C), 100% female

54.4 yrs (eligible range 40–65 yrs)

  • Iyengar yoga, 12 weeks, 2x/week

  • Intervention focused on poses thought to be beneficial for fatigue, including passive inversions, backbends, and restorative poses.

Health education

Baseline, post-intv, 3 mo FU

Fatigue (FSI)

Y > C at post-intv and 3 mo FU

1.5

Vitality (MFSI-SF)

Y > C at post-intv and 3 mo FU

1.2

Depression (BDI-II)

Y > C at post-intv only

NR

Sleep Quality (PSQI)

NS

NR

Carson (2009)

Breast cancer survivors with hot flashes

Mean = 4.9 yrs post-diagnosis (SD = 2.4)

37 (17Y, 20C), 100% female

54.4 yrs (SD = 7.5)

“Yoga of Awareness” program, 8 weeks, 1x/week

Wait list

Baseline, post-intv, 3 mo FU

Fatigue (daily diary)

Y > C at post-intv and 3 mo FU

NR

Intervention focused on postures thought to be beneficial for hot flashes, fatigue, and mood disturbance. Described as “gentle stretching poses,” done either on mat or in chair. Intervention also included breathing, study, and group discussion.

Vigor (daily diary)

Y > C at post-intv and 3 mo FU

NR

Joint pain (daily diary)

Y > C at post-intv and 3 mo FU

NR

Sleep disturbance (daily diary)

Y > C at post-intv only

NR

**note that hot flashes also improved in yoga group vs. controls

Culos- Reed (2006)

Mixed cancer survivors, 85% breast

Mean = 55.95 months post- diagnosis

38 (20Y, 18C), 92% female

51.2 yrs (SD = 10.3)

  • Yoga, 7 weeks, 1x/week

  • Intervention described as gentle stretching and strengthening exercises, included poses and breathing.

Wait list

Baseline, post-intv

Physical function (EORTC QLQ-C30)

NS

NR

Pain (EORTC QLQ-C30)

NS

NR

Fatigue (EORTC QLQ-C30 and POMS)

NS

NR

Vigor (POMS)

NS

NR

Depression (POMS)

Y > C (trend)

NR

Sleep disturbance (EORTC QLQ-C30 )

NS

NR

Kiecolt- Glaser (2013)

Breast cancer survivors

Mean = 10.9 months post- treatment (SD = 7.9)

200 (100Y, 100C), 100% female

51.6 yrs (SD = 9.2); range 27–76 yrs

  • Hatha-based yoga, 12 weeks, 2x/week

  • Intervention focused on postures thought to improve depression, fatigue, and immune function. Included poses on the floor, standing poses, and restorative poses.

Wait list

Baseline, post-intv, 3 mo FU

Fatigue (MFSI-SF)

NS at post-intv; Y > C at 3 mo FU

0.22 at post-intv; −0.36 at FU

Depression (CESD)

NS

−0.13 at post-intv; −0.16 at FU

Vitality (SF-36)

Y > C at post-intv and 3 mo FU

0.31 at post-intv; 0.32 at FU

Sleep quality (PSQI)

Y > C at post-intv and 3 mo FU

NR

Littman (2011)

Breast cancer survivors with BMI > or = 24

Y: Mean = 6 yrs post-diagnosis; C: Mean = 6.5 yrs post-diagnosis (range = 0.5–22.9 yrs)

63 (32Y, 31C), 100% female

Y: 60.6 yrs (SD = 7.1); C: 58.2 yrs (SD = 8.8); eligible range 21–75 yrs

  • Hatha-based yoga, 6 months, 5x/week

  • Intervention based on viniyoga, a Hatha-based therapeutic style of yoga, developed for overweight/ obese cancer survivors. Poses included seated and standing poses; also breathing and meditation.

Wait list

Baseline, post-intv

Physical well-being (FACT)

NS

NR

Functional well-being (FACT)

NS

NR

Fatigue (FACIT)

NS

NR

Mustian (2013)

Mixed cancer survivors, 75% breast, with sleep problems

Mean = 16.3 months since first treatment (SD = 0.85)

410 (206Y, 204C), 96% female

54.1 yrs (SE = .51)

Hatha and restorative-based yoga, 4 weeks, 2x/week

Wait list

Baseline, post-intv

Global sleep quality (PSQI)

Y > C

NR

Intervention included seated, standing, and supine poses, with emphasis on restorative poses. Also included breathing and mindfulness.

Abbreviations: BDI-II = Beck Depression Inventory II; C= Control group; CESD = Center for Epidemiologic Studies-Depression Scale; EORTC QLQ-30 = European Organization for Research and Treatment of Cancer-Quality of Life; FACIT = Functional Assessment of Chronic Illness Therapy; FACT = Functional Assessment of Cancer Therapy; FSI =Fatigue Symptom Inventory; FU = Follow- up; intv = intervention; MFSI-SF = Multidimensional Fatigue Symptom Inventory-Short Form; mo = month; NR = not reported; NS = non-significant; PSQI = Pittsburgh Sleep Quality Index; POMS = Profile of Mood States; SD = standard deviation; SF-36 = Short-Form Health Survey; Y = Yoga group.

* Follow-up data calculated as time since intervention completion.

** We focus here on physical and behavioral symptoms; many trials also included other outcomes.

*** Statistical significance was defined as p < .05.

We identified seven published RCTs that met these criteria. Most of the trials were quite small, and only two had sample sizes larger than 100. All but one used a wait-list control group. In terms of participant characteristics, the samples were primarily composed of breast cancer survivors; five studies included only breast cancer survivors, and two included a heterogeneous sample of cancer survivors that consisted primarily of women with breast cancer. The average age of study participants ranged from 51.2 to 62.9 years old.

The yoga interventions evaluated in these reports ranged from 4 weeks (Mustian et al., 2013) to 6 months (Littman et al., 2012), though most were in the 8–12-week range with classes held two times per week. Interventions were typically based on Hatha yoga and included postures and breathing exercises. Some also included meditation (Littman et al., 2012) or mindfulness (Mustian et al., 2013), and one study included study and group discussion (Carson et al., 2009). One of the notable features of these trials is that many focused on particular problems or symptoms, rather than addressing general quality of life. This focus guided enrollment and intervention content, as the interventions emphasized poses thought to be beneficial for the symptom of interest. For example,

Bower et al. (2012) enrolled breast cancer survivors who reported persistent cancer-related fatigue and tested an Iyengar-based intervention that focused on postures thought to address this symptom (i.e., supported back bends and inversions). Similarly, Carson and colleagues (2009) enrolled breast cancer survivors who were experiencing hot flashes and tested an intervention that targeted this symptom. Many of the practices were gentle or restorative in nature, though others were more physically demanding (e.g., Banasik et al., 2011).

Intervention Effects

When evaluating intervention effects, we focused on differences between the yoga and control groups at post-intervention. Overall, the most consistent positive effects were seen for fatigue and sleep disturbance. Six trials reported effects on fatigue, with four showing beneficial effects on this outcome in the yoga group versus controls. Of note, three of the four studies that found positive results specifically targeted fatigued survivors and/or included poses that targeted this symptom (Bower et al., 2012; Carson et al., 2009; Kiecolt-Glaser et al., 2014). Further, the study by Bower and colleagues included an active control condition to control for nonspecific aspects of the intervention, providing a more stringent evaluation of intervention efficacy. In the fourth positive study, a small (n = 19) trial conducted by Banasik and colleagues (2011) that used a physically demanding, Iyengar-based intervention, fatigue was the only outcome that improved. In contrast, the two trials that did not show beneficial effects on fatigue also found no effects on other outcomes (Culos-Reed et al., 2006; Littman et al., 2012). The study by Littman and colleagues emphasized home practice and recommended that participants attend one facility-based class per week along with four weekly sessions of home practice. Those who attended more facility-based classes, which was standard for the other trials, showed greater reductions in fatigue over the 6-month intervention period.

A similar pattern of results was observed for sleep disturbance. Of the four trials that reported effects on sleep, three showed beneficial effects for yoga versus controls. One of these trials specifically focused on sleep and showed improvements in both self-reported sleep quality and objective sleep measures, as well as decreased use of sleep medications (Mustian et al., 2013).

More mixed results were seen for other outcomes, including depressive symptoms, pain, and physical function. Of the three studies that reported effects on depressive symptoms, only one reported positive results (Bower et al., 2012), which appeared to be time limited. Specifically, Bower and colleagues found that yoga led to a greater decrease in depressive symptoms than health education immediately post-treatment, but this difference disappeared by the 3-month follow-up. Of the two studies that reported effects on pain, only one found positive results (Carson et al., 2009). In this case, the trial that yielded positive effects specifically targeted breast cancer survivors with hot flashes, many of whom also experience joint pain, and found that daily reports of joint pain improved in the yoga group relative to wait-list controls. In contrast, the study that reported negative results assessed general pain and pain-related impairment, and saw no effects (Culos-Reed et al., 2006). In terms of physical function, three trials assessed physical and/or functional well-being using validated quality of life measures (EORTC, FACT). None of these trials found positive effects of yoga on these outcomes. Of note, two of these trials did not find positive effects on any outcome (Culos-Reed et al., 2006; Littman et al., 2012).

Summary of Results

Overall, findings from these trials suggest that yoga is a feasible, acceptable, and safe intervention for cancer survivors. Three of the studies reviewed included information about adverse events (Bower et al., 2012; Kiecolt-Glaser et al., 2014; Mustian et al., 2013); among the 641 individuals included in these trials, only three intervention-related events were reported, which were recurrence of chronic back and/or shoulder problems. It is important to note that most of these trials used highly trained yoga instructors and administered carefully designed, “gentle” intervention protocols, which likely contributed to the lack of adverse events.

In terms of efficacy, the most consistent beneficial effects were seen for fatigue and sleep disturbance. Only a few trials assessed depressive symptoms or pain, and findings were quite mixed. This is interesting because the broader literature on yoga has reported positive effects on depression and pain (Cramer et al., 2013), although these trials focused on patients who were experiencing clinically relevant levels of these symptoms (e.g., individuals with clinically diagnosed musculoskeletal conditions). In contrast, none of the studies with cancer survivors reviewed here specifically recruited patients with elevated pain or depressive symptoms. In general, targeted yoga trials appear to be more effective.

The lack of effects on physical function were notable, particularly since this is an area where older survivors show more pronounced impairments. It is possible that longer interventions may be required to improve physical function (e.g., Oken et al., 2006), or that combined interventions that include strength training in addition to yoga may be more effective. We would encourage investigators to include objective measures of physical function, including performance-based measures (in addition to self-report) in future yoga trials.

Mindfulness Interventions: Effects on Behavioral and Physical Symptoms in Cancer Survivors

Description of Interventions

We identified 14 mindfulness-based RCTs that assessed effects on self-reported behavioral symptoms and/or physical and functional well-being in cancer survivors. Most trials were conducted with breast cancer survivors, and four (Andersen et al., 2013; Foley et al., 2010; Henderson et al., 2012; Speca et al., 2000) included patients as well as post-treatment survivors. Five interventions targeted a specific population or symptom: one for younger breast cancer survivors (Bower et al., 2015), two for survivors with cancer-related fatigue (Johns et al., 2015; Van der Lee et al., 2012), and two for survivors with sleep disturbance (Garland et al., 2014; Nakamura et al., 2013). The average age of participants ranged from 46 to 59 years. All but three trials (Garland et al., 2014; Henderson et al., 2012; Nakamura et al., 2013) used a wait-list control group.

The studies included in this review were modeled after two of the most common standardized mindfulness programs, mindfulness-based stress reduction (MBSR) and mindfulness-based cognitive therapy (MBCT) (Kabat-Zinn, 1990; Teasdale et al., 1995). In general, mindfulness interventions teach individuals to cultivate mindfulness and bring attention to present-moment experiences with openness, curiosity, and non-judgment (Kabat-Zinn, 1990). Most include psychoeducation, group discussion, informal and daily home practice, and meditation exercises (e.g., mindful breathing, sitting/walking meditation, mindful Hatha yoga). In contrast to yoga interventions, gentle yoga in this context is used primarily as a means to foster mindful awareness of the body. The majority of the reviewed trials were modified in some way to address the specific needs of cancer survivors, for example, by providing education about maintaining health and preventing cancer recurrence (Bower et al., 2015) or by discussing body image and sexuality concerns (Lerman et al., 2012). Many of the interventions were also shorter than the standard 8-week MBSR intervention. A more detailed overview of the studies, including effects on the symptoms of interest, is presented in Table 30.2.

Table 30.2. Description of Randomized Controlled Mindfulness-Based Interventions

Author, Year

Population

Time Post- Diagnosis or Treatment

Number of Participants (Mindfulness, Control), % Female

Age (Mean)

Intervention Type and Duration

Control Group

Assessments*

Outcomes**

Between Group Difference ***

Effect Size for Between Group Difference (Cohen’s D)

Andersen (2013); Würtzen (2013)

Breast cancer patients and survivors

Mean = 7.68 months since diagnosis (SD = 5.05)

336 (168M, 168C), 100% female

54.14 yrs (SD = 10.3), eligible range 18–75 yrs

  • MBSR, 8 weeks, 1x/week, 5-hr silent retreat

  • MBSR includes mindfulness meditation exercises, group discussion, emphasis on mindfulness in daily living and practice, didactic material on relations between stress and health.

Usual care

Baseline, post-intv, 4 and 10 mo FU

Sleep problems (MOS-SS)

M > C at post-intv only

0.24

Depression (CESD)

M > C at post-intv, 4 and 10 mo FU

NR

Depression (SCL-90R)

M > C (trend) at post-intv, M > C at 4 and 10 mo FU

NR

Bower (2014)

Breast cancer survivors diagnosed at or before age 50

Mean = 4.1 years since diagnosis (SD = 2.43)

71 (39M, 32C), 100% female

46.83 yrs (SD = 7.27), range 28–60 yrs

Mindful awareness practices (MAPs) program tailored for younger survivors; 6 weeks, 1x/week, no retreat

Wait list

Baseline, post-intv, 3 mo FU

Pain (BCPT)

NS

NR

MAPs is a standardized program that cultivates formal and informal mindfulness; also provided education on health and preventing cancer recurrence.

Fatigue (FSI)

M > C at post-intv only

NR

Depression (CESD)

M > C (trend) at post-intv only

0.54

Sleep quality (PSQI)

M > C at post - intv only

NR

Bränström (2010, 2012)

Mixed cancer survivors, 76% breast

49 participants diagnosed within last 2 years; 22 diagnosed more than 2 years ago.

71 (32M, 39C), 99% female

51.8 yrs (SD = 9.86), range 30–65 yrs

MBSR, 8 weeks, 1x/week, no retreat

Wait list

Baseline, post-intv, 3 mo FU

Depression (HADS)

M > C (trend) at post-intv only

0.28

Intervention followed MBSR curriculum but had no retreat

Foley (2010)

Mixed cancer patients and survivors, 42% breast

M: Mean = 2.2 yrs post-diagnosis (SD = 2.56); C: Mean = 2 yrs post-diagnosis (SD = 4.08)

115 (55M, 60C), 77% female

55.18 yrs (SD = 10.6) range 24–78 yrs

MBCT, 8 weeks, 1x/week, 5-hr silent retreat

Wait list

Baseline, post-intv, 3 mo FU

Depression (HAM-D)

M > C at post-intv and 3 mo FU

1.41

MBCT is similar to MBSR but incorporates elements of cognitive therapy; in this trial, didactic material was modified to address challenges often faced in the cancer context.

Garland (2014)

Mixed cancer survivors, 48% breast, with sleep disturbance

Mean = 3.19 yrs post-diagnosis (SD = 4.03), range = 0.17–30 yrs

111 (64M, 47C), 72% female

58.9 yrs (SD = 11.08), range 35–88 yrs

Mindfulness-based cancer recovery (MBCR), 8 weeks, 1x/week, 6-hr silent retreat

Cognitive behavioral therapy for insomnia (C)

Baseline, post-intv, 3 mo FU

Sleep disturbance (ISI)

C > M over the two post-intv assessments

NR

MBCR is a standardized program modeled after MBSR, and adapted for cancer patients and survivors (e.g., highlights challenges often faced by cancer survivors).

Sleep quality (PSQI)

C > M over the two post-intv assessments

NR

Henderson (2012)

Breast cancer patients and survivors

Diagnosed within last 2 yrs

163 (53M, 58C, 52NEP), 100% female

49.8 yrs (SD = 8.4), range 20–65 yrs

MBSR, 7 weeks, 1x/week, 7.5-hr silent retreat; plus three monthly sessions following the intervention

Nutrition education program (NEP); Usual Care (C)

Baseline, post-intv, 8 mo and 20 mo FU

Depression (SCL-90R)

M > NEP at post-intv only

NR

Depression (BDI)

NS

NR

Hoffman (2012)

Breast cancer survivors, seeking psychological services

M: Mean = 17.4 months post-diagnosis (SD = 13) C: Mean = 18.9 months post-diagnosis (SD = 15)

229 (114M, 115C), 100% female

M: 49 yrs (SD = 9.26); C: 50.1 yrs (SD = 9.14); eligible range 18–80 yrs

  • MBSR, 8 weeks, 1x/week, 6-hr silent retreat

  • Intervention closely followed MBSR.

Wait list

Baseline, post-intv, 1 mo FU

Functional well-being (FACT-B)

M > C at post-intv and 1 mo FU

NR

Physical well-being (FACT-B)

M > C at post-intv and 1 mo FU

NR

Fatigue (POMS)

M > C at post-intv and 1 mo FU

NR

Vigor (POMS)

M > C at post-intv and 1 mo FU

NR

Depression (POMS)

M > C at post-intv only

NR

Johns (2015)

Mixed cancer survivors, 85.7% breast, with fatigue

Mean = 51.3 months post-treatment (SD = 39.3)

35 (18M, 17C), 94% female

M: 58.8 yrs (SD = 9.3); C: 55.7 yrs (SD = 9.3)

  • MBSR - CRF, 7 weeks, 1x/week, no retreat

  • Intervention closely followed MBSR but was adapted to the cancer context and included psychoeducation related to cancer-related fatigue.

Wait list

Baseline, post - intv, 1 mo FU (6 mo FU for mindfulness group only)

Fatigue severity (FSI)

M > C at post-intv and 1 mo FU

−1.55 at post-intv; −1.54 at FU

Fatigue interference (FSI)

M > C at post-intv and 1 mo FU

−1.43 at post-intv; −1.34 at FU

Vitality (SF-36)

M > C at post-intv and 1 mo FU

1.29 at post-intv; 1.73 at FU

Depression (PHQ-8)

M > C at post-intv and 1 mo FU

−1.3 at post-intv; −1.71 at FU

Sleep disturbance (ISI)

M > C at post-intv and 1 mo FU

−0.74 at post-intv; −1.0 at FU

Lengacher (2009, 2012)‡

Breast cancer survivors

Mean = 18.8 weeks post-treatment (SD = 17.4)

84 (41M, 43C), 100% female

57.5 yrs (SD = 9.4), 27% > = 65 years

  • MBSR - BC (Breast Cancer), 6 weeks, 1x/week, no retreat

  • MBSR - BC includes original MBSR material but highlights psychological and physical symptoms common for breast cancer survivors (e.g. fear of recurrence, pain).

Wait list

Baseline, post-intv

Physical functioning (MOS-SF)

M > C

NR

Physical health–role limitations (MOS-SF)

M > C

NR

Pain (MOS-SF, MDASI‡)

M > C (trend) NS‡

NR

Energy (MOS-SF)

M > C

NR

Fatigue (MDASI)‡

M > C

NR

Depression (CESD)

M > C

NR

Sleep disturbance (MDASI)‡

NS

NR

Lengacher (2015)

Breast cancer survivors

Between 2 weeks and 2 years post- treatment

79 (38M, 41C), 100% female

57 yrs (SD = 9.7)

MBSR - BC, 6 weeks, 1x/week, no retreat

Wait list

Baseline, post-intv, 6 week FU

Sleep quality (PSQI)

NS

NR

Lerman (2012)

Mixed cancer survivors, 70.6% breast

M: Mean = 3.9 yrs post-diagnosis (SD = 5.1); C: Mean = 3.7 yrs post-diagnosis (SD = 3.5)

77 (53M, 24C), 100% female

M: 57.5 yrs (SD = 10.5); C: 56.4 yrs (SD = 9.8)

MBSR-based cancer recovery and wellness intervention, 8 weeks, 1x/week, 4-hr retreat

Wait list

Baseline, post-intv

Functional quality of life (EORTC QLQ-30)

NS

NR

Intervention included group discussion on body image and sexuality; used mindful breast self - examination and writing.

Nakamura (2013)

Mixed cancer survivors, 54% breast, with sleep disturbance

M: Median = 2.8 yrs post- diagnosis; MB: Median = 3.6 yrs post- diagnosis; SH: Median = 4.17 yrs post-diagnosis

57 (20M, 19MB, 18SH), 75% female

M: 50.8 yrs (SD = 9.1); MB: 55.4 yrs (SD = 9.6); SH: 51.6 yrs (SD = 10.7); eligible range 18–75 yrs

  • Mindfulness Meditation (MM), 3 weeks, 1x/week, no retreat

  • MM is a shortened version of MBSR, with no yoga, optional homework, and an expressive writing exercise. Group discussion was adapted to address sleep and cancer in relation to mindfulness.

Mind– Body Bridging (MB); Sleep Hygiene Education (SHE)

Baseline, post-intv, 2 mo FU

Sleep disturbance (MOS-SS)

M > SHE (trend) at post-intv; M > SHE at 2 mo FU

0.7

Depression (CESD)

NS

0.06

Speca (2000)

Mixed cancer patients and survivors, 42% breast

Open to participants at any stage, at any point in treatment; no mean/range given

109 (61M, 48C), 79% female

51 yrs; range 25–75 yrs

MBSR, 7 weeks, 1x/week, no retreat

Wait list

Baseline, post-intv

Vigor (POMS)

M > C

NR

Intervention modeled after MBSR, adapted for cancer patients and survivors.

Fatigue (POMS)

NS

NR

Depression (POMS)

M > C

NR

Van der Lee (2012)

Mixed cancer survivors, 58% breast, with fatigue

Mean = 3 yrs post- treatment (SD = 2.3)

100 (72M, 28C), 86% female

53.1 yrs (SD = 9.1)

MBCT, 8 weeks, 1x/week, 6hr retreat, follow-up session at 2 months post-intv

Wait list

Baseline, post-intv (6 mo FU for MBCT group only)

Fatigue severity (CIS)

M > C at post-intv

0.74

MBCT is similar to MBSR but includes elements of cognitive therapy, such as learning to identify and detach from negative thoughts; this trial also included didactic material on fatigue.

Functional impairment (SIP)

NS

NR

Abbreviations: BCPT = Breast Cancer Prevention Trial Symptom Checklist; C= Control group; CESD = Center for Epidemiologic Studies-Depression Scale; CIS = Checklist Individual Strength; CRF = Cancer-related fatigue; EORTC QLQ-30 = European Organization for Research and Treatment of Cancer-Quality of Life; FACT-B = Functional Assessment of Cancer Therapy-Breast Symptom Index; FSI =Fatigue Symptom Inventory; FU = Follow-up; HADS = Hospital Anxiety and Depression Scale; HAM-D = Hamilton Rating Scale for Depression; intv = intervention; ISI = Insomnia Severity Index; M = Mindfulness group; MAPs = Mindful Awareness Practices; MBCT = Mindfulness-Based Cognitive Therapy; MBSR = Mindfulness-Based Stress Reduction; MDASI = M.D. Anderson Symptom Inventory; mo = month; MBB = Mind–Body Bridging; MOS-SF = Medical Outcomes Study Short-Form General Health Survey; MOS-SS = Medical Outcomes Study Sleep Scale; NEP = Nutrition Education Program; NR = not reported; NS = non-significant; PHQ-8 = Patient Health Questionnaire; PSQI = Pittsburgh Sleep Quality Index; POMS = Profile of Mood States; SD = standard deviation; SF-36 = Short-Form Health Survey; SHE = Sleep Hygiene Education; SIP = Sickness Impact Profile.

* Follow-up data calculated as time since intervention completion.

** We focus here on physical and behavioral symptoms; many trials also included other outcomes.

*** Statistical significance was defined as p < .05.

Andersen 2013 and Würtzen 2013 report from the same randomized controlled trial; Würtzen 2013 results are indicated with a dagger symbol.

Lengacher 2009 and Lengacher 2012 report from the same randomized controlled trial; Lengacher 2012 results are indicated with a double dagger symbol.

Intervention Effects

Across studies, the most consistent positive effects were seen for fatigue and depression. All of the six studies that assessed fatigue found improvements in fatigue, energy, vigor, or vitality in the mindfulness group versus controls at post-intervention. The sustained and clinically significant effects seen in the trials by Van der Lee and Garssen (2012) and Johns and colleagues (2015) are particularly notable. Both interventions targeted survivors with cancer-related fatigue and provided brief psychoeducation on the relation between cancer and fatigue. While Johns et al. (2015) used a modified MBSR program, Van der Lee et al. (2012) used a modified MBCT program that included elements of cognitive therapy, but omitted gentle yoga. The success of both programs suggests that targeted mindfulness interventions are beneficial in addressing fatigue in this population, despite variations in approach.

Similarly, 9 of the 10 trials that examined effects on depressive symptoms found improvements in this outcome at post-intervention (three marginally so: Bower et al., 2015; Bränström et al., 2010; Wurtzen et al., 2013). The one study that did not see a significant effect for mindfulness meditation was an abbreviated 3-week intervention, and it still noted significant within-group improvement (Nakamura et al., 2013). These positive effects on depression are consistent with the broader literature on mindfulness for cancer patients and other clinical populations (Goyal et al., 2014; Ledesma & Kumano, 2009). However, improvements were not consistently maintained in the months after treatment completion. Only three out of eight studies that included a follow-up assessment saw sustained improvement in depression (Foley et al., 2010; Johns et al., 2015; Würtzen et al., 2013). It may be worthwhile to consider whether modifications such as booster sessions or online programs can facilitate enduring practice and continued improvement in well-being.

The seven studies assessing subjective sleep quality showed more mixed effects. Five of these studies compared mindfulness interventions to a wait-list control group; three reported significantly reduced sleep problems in the mindfulness group versus controls at post-intervention (Andersen et al., 2013; Bower et al., 2015; Johns et al., 2015), and two found no group differences in subjective sleep problems at post-intervention (Lengacher et al., 2012; Lengacher et al., 2015). The remaining two trials targeted survivors with sleep disturbance, and both found mindfulness to show weaker or delayed effects in comparison to an active comparison group. In the study conducted by Nakamura and colleagues (2013), “Mind–Body Bridging” was more effective than mindfulness meditation at post-intervention, although both were superior to sleep hygiene education at a 2-month follow-up. In a comparative effectiveness trial, Garland and colleagues (2014) randomized participants to a mindfulness-based cancer recovery program (MBCR) or cognitive-behavioral therapy for insomnia (CBT-I). They found that CBT-I improved subjective sleep quality significantly more than the mindfulness program at post-intervention and at a 3-month follow-up. The mindfulness group did demonstrate clinically relevant improvement at the follow-up; however, the CBT-I worked more quickly and had more lasting and robust effects.

The evidence that mindfulness interventions improve physical function and symptoms in cancer survivors is similarly mixed. Four studies assessed self-reported physical and functional well-being, and two saw improvement for the mindfulness group versus controls on these outcomes (Hoffman et al., 2012; Lengacher et al., 2009). In addition, two studies conducted with breast cancer survivors assessed and found improvements in menopausal symptoms (Bower et al., 2015; Hoffman et al., 2012). This is a notable finding, as these symptoms often result from endocrine therapy, and may be associated with non-adherence to treatment (Murphy et al., 2012).

By contrast, mindfulness interventions have not demonstrated positive effects on pain in cancer survivors. Neither of the two trials assessing musculoskeletal pain (Bower et al., 2015) and bodily pain/pain severity (Lengacher et al., 2009; Lengacher et al., 2012) found significant improvement. Both trials did show effects on other symptoms, suggesting that they were generally effective interventions. These results are somewhat surprising, as mindfulness was initially proposed as a way to facilitate self-regulation of stress and chronic pain (Kabat-Zinn, 1990). Further, a recent meta-analysis found moderate evidence for pain improvement in clinical populations following mindfulness meditation (Goyal et al., 2014).

Summary of Results

Overall, results from these trials suggest that mindfulness-based interventions are safe, feasible, and acceptable for older cancer survivors. No adverse effects were found in the few studies that reported on them. In terms of efficacy, mindfulness showed consistently positive effects on fatigue and depressive symptoms, mixed evidence for effects on sleep and physical function, and no effect on pain. Several studies noted an association between the extent of mindfulness practice and positive treatment effects (Hoffman et al., 2012; Lengacher et al., 2009; Lerman et al., 2012; Speca et al., 2000), suggesting that there may be a dose-response relationship. It is important to note that none of these trials specifically targeted older survivors, though individuals up to age 88 were included in the research.

Summary

Our review of the literature on yoga and mindfulness-based therapies for cancer survivors suggests that these approaches are feasible, acceptable, and safe for this population, and may lead to improvements in fatigue, sleep problems, and depression (mindfulness-based interventions only).

It is important to note that this is a developing area of research, and many of the studies included in this review were designed to provide an initial demonstration of intervention feasibility and preliminary efficacy, rather than a definitive evaluation of intervention effects. As such, many were limited by small sample sizes, single-site design, use of wait-list control conditions, and limited (if any) follow-up. The studies are also limited in generalizability, due to the overrepresentation of breast cancer survivors and underrepresentation of minorities. In addition, poor or incomplete reporting of statistical analyses rendered a number of studies difficult to evaluate. Future studies that use multisite designs (e.g., Carlson et al., 2013) with longer-term follow-up (e.g., Andersen et al., 2013) and active control conditions (e.g., Bower et al., 2012) and that include more representative samples of cancer survivors will allow a clearer evaluation of the effectiveness and durability of these interventions. Although we focused here on self-report measures, which are the gold standard for assessing subjective physical and behavioral symptoms, several trials also assessed relevant objective measures (e.g., actigraphy, physical performance measures); inclusion of these measures in future research would enhance our understanding of intervention effects.

In addition to these general recommendations, we believe that interventions may be enhanced by consideration of the specific needs and issues faced by older cancer survivors. In many cases, interventions have already been adapted for individuals with cancer (e.g., mindfulness-based cancer recovery); additional modifications for older survivors may improve the efficacy of these interventions and ensure safety in this potentially vulnerable group. Several mindfulness-based and yoga interventions have already been designed to accommodate older adults (e.g., Morone & Greco, 2014; Park et al., 2014), which could be used to inform programs targeting older cancer survivors. For mindfulness-based interventions, very simple and minor changes are typically made. For example, sitting meditation and mindful yoga may be done in chairs rather than on the floor, and participants with hearing difficulties sit closer to the instructor. Given the physical nature of yoga interventions, more extensive modifications may be required. In general, older adults are at greater risk for musculoskeletal side effects from yoga, and this may be exacerbated in cancer survivors who have undergone treatments that may accelerate biological aging processes. For example, treatment with aromatase inhibitors in women with breast cancer and treatment with androgen deprivation therapy in men with prostate cancer can accelerate bone loss and increase risk of fractures (Naeim et al., 2014). Thus, yoga interventions focusing on older cancer survivors need to be carefully designed to minimize these risks, including safety screening of potential participants, careful selection and sequencing of poses, detailed pose modifications for participants with physical limitations, and use of instructors who have experience with both cancer survivors and older adults, among other considerations (Krucoff et al., 2010). Preliminary work suggests that modified yoga programs are effective for older individuals (e.g. Morone & Greco, 2014; Park et al., 2014), supporting their potential usefulness with older cancer survivors.

Although our review has focused on behavioral and physical outcomes, yoga and mindfulness may also lead to improvements in aspects of psychological functioning relevant for older survivors, including reduced fear of recurrence and enhanced perceptions of peace and meaning in life (Bower et al., 2015; Lengacher et al., 2009). In addition, these approaches may influence cancer-relevant biological outcomes, including inflammatory processes. A growing body of research suggests that mind–body therapies, including yoga, mindfulness, and tai chi/qi gong, may reduce inflammatory activity (Morgan et al., 2014), and work conducted by our group suggests that these effects may extend to cancer survivors. For example, we have shown that yoga (Bower et al., 2014), mindfulness (Bower et al., 2015), and tai chi (Irwin et al., 2014) are associated with reduced inflammatory signaling in randomized controlled trials conducted with breast cancer survivors. There is also evidence that mind–body therapies may have positive effects on other biological processes relevant for older cancer survivors, including anti-viral immunity (Morgan et al., 2014) and biomarkers of bone health (Jahnke et al., 2010).

Cancer survivors are avid consumers of mind–body therapies, and these approaches may offer considerable benefits for this large and growing population. We recommend that researchers and clinicians carefully consider the use of mind–body approaches for older cancer survivors and develop targeted approaches that address the needs of this group in creative and thoughtful ways. For example, investigators may want to consider combining strength training with mind–body approaches to enhance effects on physical outcomes. Along these lines, although not considered in this review, tai chi/qi gong may be an attractive mind–body option for older cancer survivors. In particular, the movements and postures in tai chi/qi gong may be a helpful way to improve balance and incorporate gentle weight-bearing exercise, both of which are increasingly important with greater age (Jahnke et al., 2010). Indeed, preliminary trials have shown beneficial effects of qi gong on mental well-being and fatigue in older survivors (e.g., Campo et al., 2014). Given the growing number of older survivors in the United States, the development and implementation of interventions that improve psychological and physical well-being in this group is of critical importance.

Funding

Julienne E. Bower was supported by the Breast Cancer Research Foundation and by NIH/NCI R01 CA160427. Chloe C. Boyle was supported by the NIH/NIMH Predoctoral Fellowship 5T32MH015750-35, “Biobehavioral Aspects of Mental and Physical Health.”

Disclosure Statement

The authors declare that they had no conflicts of interest with respect to their authorship or the publication of this article.

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