Background
Cancer is the second leading cause of death in the United States.1 With advances in cancer screening and treatment, survival rates have increased by 20% over the past 4 decades.2 Despite increased survival rates, quality of life (QoL) is often dramatically diminished due to cancer-related and treatment-related toxicities.3–6
Cancer-related fatigue (CRF) is one of the most pervasive toxicities experienced by survivors.5,7–11 Although most patients experience CRF during treatment, up to 40% of survivors continue experiencing this debilitating fatigue after completion of treatment.12–17 These survivors often report a lack of energy, tiredness, and a need to slow down and rest, which interferes with their ability to work, resume daily routines (eg, walking), and engage in physical activity (PA).6,18
Evidence suggests that yoga alleviates a variety of cancer-induced and treatment-induced toxicities, and could, therefore, improve QoL among cancer survivors.19–32 We previously showed that our yoga intervention, Yoga for Cancer Survivors (YOCAS), effectively improves CRF, insomnia, cognitive impairment, arthralgias, and pain among cancer survivors.33–37 To our knowledge, no nationwide, multicenter, phase III randomized controlled trial (RCT) has studied how reducing CRF through yoga consequently influences CRF’s interference with survivors’ daily activities such as walking and engaging in PA and QoL. Here we report the effect of YOCAS on CRF’s interference with survivors’ walking, PA, and QoL as secondary outcomes from our phase III RCT, and examine whether yoga-induced improvements in CRF mediate changes in CRF’s interference with walking, PA, and QoL among survivors.
Patients and Methods
Study Design
We used data collected from our nationwide, multicenter, phase III RCT (ClinicalTrials.gov identifier: NCT00397930) conducted via the University of Rochester Cancer Center NCI Community Oncology Research Program Research Base (URCC NCORP RB) to examine the effect of YOCAS on CRF’s interference with walking, PA, and QoL (as secondary outcomes) among cancer survivors. The primary and other secondary outcomes along with detailed study design and methods have been published previously.33–37 See supplemental eAppendix 1 (available with this article at JNCCN.org) for information on study recruitment and randomization.
Participants
Participant inclusion criteria included (1) any type of cancer diagnosis, excluding a metastatic diagnosis; (2) completion of primary treatment 2 to 24 months prior to enrollment; (3) persistent sleep disturbance (≥3 on symptom inventory scale); (4) age ≥21 years; and (5) ability to read and understand English. Participants were excluded if they (1) regularly practiced yoga within 3 months or planned to start a new yoga program during the study period; (2) were diagnosed with sleep apnea or metastatic cancer; and (3) were currently receiving any form of cancer treatments except hormonal therapy.
Yoga Intervention
YOCAS is a standardized 4-week yoga intervention that is based on gentle hatha and restorative yoga consisting of breathing exercises, physical alignment postures, and mindfulness exercises.33 Participants in the YOCAS group received 8 yoga sessions (75 minutes per session, twice per week) at low to moderate intensity. Each yoga session was delivered by a Yoga Alliance–registered instructor in a group setting (10–15 participants per group) at community-based sites (eg, community centers, cancer centers, and yoga studios).33
To ensure the standardization, quality, and fidelity of the yoga intervention, each instructor completed a 2-hour training session conducted by the URCC NCORP RB and was instructed to follow the provided intervention manual and a DVD to deliver YOCAS sessions. The study coordinator from each participating NCORP community oncology practice also attended a randomly selected yoga session to observe and verify whether proper content was delivered.
Standard Care Control
Participants in the standard care control group continued their usual follow-up clinic visits with their oncologists and primary care providers. They received the same amount of time and attention from the research team regarding study measures but had no yoga exposure.
Measures
Medical records were reviewed to confirm participants’ eligibility and collect clinical information (eg, cancer type, previous treatment). Demographic data were collected via the study-specific form. Race data were collected using the NCI Clinical Trials Reporting Program criteria for clinical trials. For data reporting purposes, we condensed racial categories to White, Black, and Other (comprising Native Hawaiian or Other Pacific Islander, Asian, American Indian, Alaska Native, and unknown).
Adherence and compliance were monitored by patient-reported daily diaries and yoga attendance logs completed by yoga instructors. A feedback form was used to collect the helpfulness of the YOCAS intervention and whether yoga participants would recommend the intervention to other survivors experiencing similar symptoms. Adverse events were monitored using NCI’s Common Terminology Criteria for Adverse Events and were reported to the URCC Data Safety Monitoring Committee.
CRF’s Interference With Walking, PA, and QoL
The symptom inventory is a commonly used and widely accepted tool for both research and clinical assessments of the severity of symptoms and how symptoms interfere with patients’ daily living.38 We modified the MD Anderson Symptom Inventory and included 12 common symptoms and 8 interference items.36,37 Participants were asked to rate the severity of each symptom on a scale of 0 to 10 (0 = not present; 10 = as bad as you can imagine) and how much their fatigue interfered with the 8 items of their life (including daily living, mood, work, relations with other people, general physical activity, walking, exercise, and quality of life) with a scale of 0 to 10 (0 = did not interfere; 10 = completely interfered). In this study, we used 3 Symptom Inventory interference items to assess CRF’s interference with walking, PA, and QoL. Higher scores indicate worse interference.
CRF
CRF was measured via the Multidimensional Fatigue Symptom Inventory-Short Form (MFSI),39,40 a validated, 30-item, commonly used fatigue instrument that generates a total score indicating overall CRF level and 5 subdomain scores indicating general, physical, emotional, and cognitive fatigue and vigor levels. Higher scores indicate worse fatigue levels. CRF results were previously published.34,37 In this study, the total MFSI scores were used for mediation analysis.
Statistical Analyses
Among 410 participants who consented and were randomized, 328 provided complete baseline and postintervention symptom inventory and MFSI data. A sample size of 328 (YOCAS: n=168; standard care: n=160) provided >90% power to detect an effect size of 0.33 in between-group differences in CRF’s interference with walking, PA, and QoL scores assuming a correlation coefficient of 0.5 between baseline and postintervention at a significance level of 5% with a 2-tailed F test using analysis of covariance (ANCOVA).
Between-group differences in baseline demographic data and characteristics were examined with 2-tailed t tests for continuous variables and chi-square tests for categorical variables. Within-group differences in CRF’s interference with walking, PA, and QoL were assessed using 2-tailed t tests. Between-group intervention effects on CRF’s interference with walking, PA, and QoL at postintervention were assessed using ANCOVA with the intervention arm as the group factor and baseline value as a covariate. Two-tailed t tests and ANCOVA were performed using SAS 9.4 (SAS Institute Inc.). The effect size was calculated using the between-group mean change (postintervention minus baseline) in CRF’s interference with walking, PA, and QoL divided by the standard deviation of baseline scores.
The mediation analysis was conducted using path modeling on change scores in CRF with change scores in CRF’s interference with walking, PA, and QoL as the dependent variables to derive path coefficients. The path modeling included a direct path between the intervention arm (YOCAS vs standard care) and each outcome variable (CRF’s interference with walking, PA, and QoL), a path between the intervention arm and CRF, and a path between CRF and each outcome variable. Statistical significance of mediation was assessed using nonparametric bootstrap 95% confidence intervals for the indirect path coefficient from the intervention arm to each outcome variable on CRF. Statistical significance was determined as P≤.05.
Data analyses followed the intent-to-treat principle and were based on complete cases (see supplemental eAppendix 1 for the description of intent-to-treat, multiple imputation, and mediation analysis).
Results
Figure 1 shows the CONSORT diagram. Among 413 survivors who consented to participate in the study, 3 were excluded due to ineligibility, 410 were randomized to either YOCAS (n=206) or standard care (n=204), 357 provided complete baseline symptom inventory and MFSI data, and 328 provided complete baseline and postintervention symptom inventory and MFSI data. Eighty-one enrolled participants, including 37 YOCAS participants and 44 standard care controls, dropped out of the study due to medical issues (n=12), personal issues (n=47), unknown reasons (n=20), and starting their own yoga program (n=2). One YOCAS participant did not provide complete baseline data. The proportion of dropouts between YOCAS (18%) and standard care (22%) was not significantly different.
CONSORT diagram.
Abbreviations: MFSI, Multidimensional Fatigue Symptom Inventory; YOCAS, Yoga for Cancer Survivors.
Citation: Journal of the National Comprehensive Cancer Network 21, 2; 10.6004/jnccn.2022.7080
Demographics and Baseline Characteristics
Table 1 shows the demographics and baseline characteristics of 357 participants (YOCAS: n=176; standard care: n=181) who provided complete baseline symptom inventory and MFSI data. Mean [SD] age of participants was 54.3 [10.2] years; most were female (96%), White (93%), married or in a committed relationship (73%), educated at a college level or higher (81%), employed (81%), and breast cancer survivors (77%). Participants had completed surgery (90%), chemotherapy (71%), and/or radiation therapy (67%) prior to enrollment. On average, there was a mean [SD] of 15.7 [8.2] months since their first cancer treatment. No significant between-group differences were found in demographics and baseline characteristics.
Demographics and Baseline Characteristics
Adherence, Compliance, and Adverse Events
YOCAS participants attended an average of 6.5 of 8 prescribed yoga sessions and reported practicing 1 additional session per week on their own. The average rating of exertion was 3.4 on a 0 to 10 scale (with 0 = “nothing at all” and 10 = “very, very strong”), indicating that the intensity of the YOCAS session was low to moderate. YOCAS participants, on average, practiced 182 minutes of yoga each week or 728 minutes across the 4-week intervention period, which was 128 minutes more than the prescribed yoga dose (eight 75-minute sessions = 600 minutes). No significant yoga contamination was found in the standard care group; 7 standard care controls reported an average of 20 minutes of yoga practice weekly during the intervention period. No study intervention–related adverse events were reported.
CRF’s Interference With Walking, PA, and QoL
YOCAS participants reported significant improvements in CRF’s interference with walking (−0.6 ± 0.2; P=.01), PA (−0.9 ± 0.2; P<.01), and QoL (−1.0 ± 0.2; P<.01) from baseline to postintervention, whereas standard care controls reported no change in these outcomes. In addition, ANCOVA revealed significantly greater improvements in CRF’s interference with walking (−0.9 ± 0.3; P<.01; effect size = −0.33; 95% CI, −0.54 to −0.11), PA (−0.9 ± 0.3; P<.01; effect size = −0.33; 95% CI, −0.52 to −0.15), and QoL (−0.9 ± 0.3; P<.01; effect size = −0.33; 95% CI, −0.51 to −0.14) in YOCAS participants than in standard care controls at postintervention, controlling for baseline values (Figure 2, Table 2). More than 90% of YOCAS participants found these changes to be clinically meaningful; they explicitly stated that the YOCAS intervention was helpful and they would recommend it to other survivors for managing these side effects.
Changes in CRF’s interference with walking, PA, and QoL. Data are presented as effect size and its 95% confidence limits.
Abbreviations: CRF, cancer-related fatigue; PA, physical activity; QoL, quality of life; YOCAS, Yoga for Cancer Survivors.
*P≤.05.
Citation: Journal of the National Comprehensive Cancer Network 21, 2; 10.6004/jnccn.2022.7080
Changes in CRF’s Interference With Walking, Physical Activity, and Quality of Life
Mediational Effect of CRF on CRF’s Interference With Walking
YOCAS participants, compared with standard care controls, reported significantly greater improvements in CRF from baseline to postintervention.34 Mediation analysis revealed that improvements in CRF significantly mediated the intervention effect on CRF’s interference with walking. The path mediation model of CRF and CRF’s interference with walking adjusted with the intervention effect is demonstrated in Figure 3. The total effect of YOCAS compared with standard care on symptom inventory walking interference score was −1.01 points (P<.01), indicating that YOCAS improved CRF’s interference with walking by 1.01 points compared with the effect of standard care on walking. Improvements in CRF significantly mediated the YOCAS effect on CRF’s interference with walking by 0.45 points in addition to the direct YOCAS effect on CRF’s interference with walking of 0.57 points, suggesting that 44% (95% CI, 24%–100%) of the improvements in CRF’s interference with walking was mediated through improvements in CRF.
Mediational effect of CRF on its interference with walking. Data are presented as regression coefficient ±SE.
Abbreviations: CRF, cancer-related fatigue; YOCAS, Yoga for Cancer Survivors.
*P≤.05.
Citation: Journal of the National Comprehensive Cancer Network 21, 2; 10.6004/jnccn.2022.7080
Mediational Effect of CRF on CRF’s Interference With PA
Mediation analysis revealed that improvements in CRF significantly mediated the intervention effect on CRF’s interference with PA. The path mediation model of CRF and CRF’s interference with PA adjusted with the intervention effect is demonstrated in Figure 4. The total effect of YOCAS compared with standard care on symptom inventory PA interference score was −1.02 points (P<.01), indicating that YOCAS improved CRF’s interference with PA by 1.02 points compared with the effect of standard care on PA. Improvements in CRF significantly mediated the YOCAS effect on improvements in CRF’s interference with PA by 0.54 points in addition to the direct YOCAS effect on CRF’s interference with PA of 0.47 points, suggesting that 53% (95% CI, 34%–100%) of the improvements in CRF’s interference with PA was mediated through improvements in CRF.
Mediational effect of CRF on its interference with PA. Data are presented as regression coefficient ±SE.
Abbreviations: CRF, cancer-related fatigue; PA, physical activity; YOCAS, Yoga for Cancer Survivors.
*P≤.05.
Citation: Journal of the National Comprehensive Cancer Network 21, 2; 10.6004/jnccn.2022.7080
Mediational Effect of CRF on CRF’s Interference With QoL
Mediation analysis revealed that improvements in CRF significantly mediated the intervention effect on CRF’s interference with QoL. The path mediation model of CRF and CRF’s interference with QoL adjusted with the intervention effect is demonstrated in Figure 5. The total effect of YOCAS compared with standard care on symptom inventory QoL interference score was −0.96 points (P<.01), indicating that YOCAS improved CRF’s interference with QoL by 0.96 points compared with the effect of standard care on QoL. Improvements in CRF significantly mediated the YOCAS effect on improvements in CRF’s interference with QoL by 0.43 points in addition to the direct YOCAS effect on CRF’s interference with QoL of 0.52 points, suggesting that 45% (95% CI, 26%–100%) of the improvements in CRF’s interference with QoL was mediated through improvements in CRF.
Mediational effect of CRF on its interference with QoL. Data are presented as regression coefficient ±SE.
Abbreviations: CRF, cancer-related fatigue; QoL, quality of life; YOCAS, Yoga for Cancer Survivors.
*P≤.05.
Citation: Journal of the National Comprehensive Cancer Network 21, 2; 10.6004/jnccn.2022.7080
Discussion
To our knowledge, this is the first nationwide, multicenter, phase III RCT demonstrating how reducing fatigue through a standardized, 4-week, yoga intervention (YOCAS) has broader implications on survivors’ daily activities and QoL. Our findings suggest that YOCAS, the gentle hatha and restorative yoga–based, low- to moderate-intensity yoga intervention, practiced 2 to 3 times per week (182 minutes per week; 32–75 minutes per session) for 4 weeks significantly improves CRF’s interference with walking, PA, and QoL among cancer survivors. A significant proportion (44%–53%) of the YOCAS effect on CRF’s interference with walking, PA, and QoL is due to improvements in CRF. By practicing YOCAS, survivors not only reported less CRF but consequently improved their engagement in daily activities such as walking and PA, and overall QoL, suggesting the broader therapeutic impact of yoga on symptom management in cancer survivors.
Although most oncology guidelines41–45 mention that it is reasonable to recommend the use of yoga for treating CRF, compelling level 1/category 1 scientific evidence from multiple blinded phase III RCTs is insufficient to make yoga a gold standard treatment. Results of this study add substantial value to the scientific evidence supporting the use of yoga for treating CRF and its interference with essential daily activities such as walking, PA, and QoL.24–26,28–30,32–37,46–48 In addition, our YOCAS participants demonstrated high adherence and compliance to the yoga intervention, found the yoga intervention helpful, and claimed they would recommend it to other survivors experiencing similar side effects, which underlines the clinically meaningful effect of yoga on symptom management.33 Because these were secondary exploratory analyses, future phase III RCTs designed a priori with CRF and its interference with walking, PA, and QoL as primary outcomes are needed.
Although the results of this study are compelling regarding the use of yoga for treating CRF and its interference with daily activities and QoL, yoga remains underprescribed as an element of supportive care among cancer survivors.49,50 Improving awareness and enhancing accessibility of yoga therapy in cancer care and collaborations with yoga therapists and integrative medicine can lead to dissemination and implementation of yoga therapy in the oncology setting and extension of the benefits of yoga to greater numbers of cancer survivors.50–53 We understand that not all survivors will want to use yoga for treating CRF and other side effects. For those patients, it is reasonable to recommend the use of other behavioral interventions noted in oncology supportive care treatment guidelines (eg, exercise, cognitive behavioral therapy).
Certain limitations should be considered when interpreting our results and developing future studies, including (1) the generalizability of the results: most of our study participants were White, female, educated at a college level or higher, and breast cancer survivors, who do not represent the diversity of the cancer population; (2) the lack of a comparison with an active behavioral placebo: the study design did not compare YOCAS with an active behavioral placebo controlling for subject contact time and attention of the intervention; therefore, we cannot assess whether the improvements in CRF and in CRF’s interference with walking, PA, and QoL are specific to YOCAS; (3) use of only 3 items of the self-reported symptom inventory questionnaire to evaluate CRF’s interference with walking, PA, and QoL might not comprehensively evaluate the true interference level; (4) CRF and the 3 main outcomes were assessed only at baseline and postintervention: this assessment arrangement could not capture temporal changes for mediation analysis and evaluate sustainability of the intervention effect; (5) although compliance with YOCAS was good in this study, the effective dose of yoga might be challenging for survivors with more severe medical, physical, financial, or environmental barriers; and (6) 20% of enrolled participants dropped out due to personal, medical, and other reasons.
Future phase II/III RCTs should consider testing yoga intervention among survivors with diverse demographic backgrounds and various cancer types and treatment histories, and develop strategies to improve participant retention. Comparing yoga intervention to known effective treatments such as exercise or psychosocial interventions for alleviating CRF and its interference with daily activities and QoL could further elucidate the magnitude of each yoga component or their combination (breathing, postures, and mindfulness) versus the active component from other interventions, provide more direct clinical evidence, and identify multiple treatment options for symptom management. Collecting and analyzing objective biophysiologic data and assessing mediational relationships might help reveal the etiologic and pathophysiologic mechanisms of CRF and its connection to survivors’ walking, PA, and QoL. The study of temporal and dose–response relationships can help oncologists and yoga therapists prescribe yoga doses more precisely. Combining yoga with other behavioral interventions can also be considered to elicit greater improvements in CRF and its interference with walking, PA, and QoL among cancer survivors.
Conclusions
Our findings suggest that the standardized 4-week YOCAS yoga program improved CRF’s interference with walking, PA, and QoL among cancer survivors. More importantly, 44% to 53% of the improvements in CRF’s interference with walking, PA, and QoL are attributable to improvements in CRF resulting from yoga. Our findings provide strong clinical evidence for oncologists to include yoga as a treatment option when designing a cancer care plan for survivors experiencing CRF and its interference with walking, PA, and QoL.
Acknowledgments
We acknowledge and thank all the cancer survivors who participated in this study, the participating NCORP community oncology practices, URCC NCORP RB staff, and Wilmot Cancer Institute Human Biopsychology Shared Resource PEAK Human Performance Clinical Research Laboratory staff for their help with this nationwide, multicenter phase III RCT. We also acknowledge and thank Drs. Susan Rosenthal and Elaine Smolock for editorial assistance.
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