The Effects of the Bali Yoga Program for Breast Cancer Patients on Cancer Related Fatigue: Results of a Randomized Partially Blinded Controlled Trial

Abstract

Background:

A few complementary and alternative medicine methods have been reported to reduce cancer related fatigue (CRF). The purpose of this study was to evaluate the effects of a yoga intervention in reducing CRF among women receiving chemotherapy.

Materials and Methods:

This was a randomized partially blinded controlled trial comparing a standardized yoga intervention to standard care. It was conducted at three medical centers in Montreal, Canada. Eligible patients were women diagnosed with stage I–III breast cancer receiving chemotherapy. Participants were randomly assigned to receive the yoga intervention immediately or after a waiting period. The Bali Yoga Program for Breast Cancer patients (BYP-BC) consisted of 24 gentle poses, 2 breathing techniques, relaxation periods, and psychoeducational themes. Participants attended eight weekly sessions lasting 90 minutes and a DVD for home practice with 20- and 40-minute sessions. Participants in the waitlist (WL) control group received standard care.

Results:

Forty-eight participants were included in the study. The repeated measure analyses revealed no significant increase in general fatigue in the BYP-BC group (P = 0.66) while it significantly worsened in the WL group (P = 0.000). Motivation improved in the BYP-BC group (P = 0.01) and worsened in the WL group (P = 0.01).

Conclusions:

These preliminary results suggest BYP-BC could be beneficial in preventing worsening of CRF during chemotherapy.

Introduction

Worldwide, breast cancer (BC) is the second most common cancer diagnosed excluding non-melanoma skin cancer.¹ Despite improved oncological treatments and survival rates, numerous studies have documented a plethora of adverse side effects and psychological burden associated with cancer diagnosis and treatment.² Fatigue is increasingly recognized as one of the most distressing symptoms for cancer patients.^3

–7

Cancer related fatigue (CRF) differs from tiredness experienced in the general population.⁸ CRF is described as an overwhelming feeling of tiredness, exhaustion, and discomfort interfering with usual functioning. It is also perceived in disproportionate levels compared to actual exertion and it is not relieved by sleep or rest.^9

–13 CRF is characterized as multidimensional, altering an individual's cognitive, physical and emotional state.^14

–17 It is estimated that more than 75% of patients complain of CRF throughout cancer treatments.^18,19 However, studies suggest CRF is underreported by patients,^2,20 and seldom routinely assessed by physicians leaving it untreated.²¹ Depression and anxiety symptoms, pain, and sleep disruption have been found to correlate with CRF frequency and severity.^{13,15,22

–27}

Many studies reveal that CRF disrupts daily functioning, leading to psychological distress and/or impaired quality of life (QoL).^20,28,29 In fact, 30% of patients having received chemotherapy complained of fatigue and reported normal daily activities hindrance.^13,30 Considering these findings, several practice guidelines have been outlined to promote CRF management.

Among them, yoga practice has seen a significant increase for cancer survivors and patients undergoing treatment.³¹ However, yoga has yielded inconsistent results with CRF management. In this regard, systematic reviews, two meta-analyses, a bibliometric study of randomized control trials and a nationwide multicenter study suggest yoga may be beneficial in reducing CRF, improving QOL, increasing physical functioning, decreasing psychological burden and improving the management of undesirable treatment side effects.^32

–37 However, several methodological drawbacks limit the extent to which yoga can be considered an effective intervention in symptom management^38,39 and a recent study and meta-analysis found no beneficial effect of yoga compared to standard care⁴⁰ or physical activity.⁴¹ Additional randomized controlled trials (RCTs) are necessary to further investigate its potential benefits.

The aim of this study is to determine the effects of a standardized yoga program for CRF among BC patients. A previous study reported the beneficial impact of the Yoga Bali Program for BC patients (BYP-BC) in reducing and preventing the worsening of depression symptoms during chemotherapy.⁴² The BYP-BC is a standardized yoga intervention based on the method of Dr. Madan Bali.⁴³ This method is a gentle form of Hatha yoga which emphasizes the healing capacity of one's body, the experiential process, and the relaxation response. To do so, Dr. Bali's method teaches the psychological, physical and physiological benefits of the yoga poses. Additionally, this method uniquely outlined a yoga pose-visualisation-rest sequence to promote the relaxation response. This method was adapted for women with breast cancer (BYP-BC) by selecting specific yoga poses (Table 1) approved by medical doctors to promote physical and psychological well-being. Additionally, eight psychoeducational themes were outlined with Dr. Bali and two psychologists to explore and understand the psychological impact of breast cancer and explain how yoga can promote psychological well-being (see materials and methods section). Lastly, to ensure the BYP-BC was standardized, each yoga teacher, formerly trained by Dr. Bali, followed an 8-week training to review the psychoeducational themes and ran a pilot group with breast cancer survivors.

Table 1.

Bali Yoga Program for Breast Cancer Poses

Yoga poses
1-Guided relaxation during corpse pose	13-Seated straight legs with forward bend
2-Full body gentle stretch	14-Butterfly+forward bend
3-Straight legs raise, rotation and stretching	15-Sideways stretch on knees and camel
4-Bent knee sideways twist	16-Child pose
5-Double straight leg raises	17-Locust, leg raises, roll on side, circles with legs behind
6-Double knee clasp, head to knees	18-Cobra+twist of head and chest, left and right
7-Double knee clasp head to knees with rocking back and forth	19-Cobra+circles with body
8-Plow	20-Cat stretch with abdominal and chin lock
9-Shoulder stand	21-Leg extensions on all fours, one leg at a time
10- Bridge with ankle clasp, rocking left to right, circle with hips	22-Child pose
11-Sit-up with straight back, circles	23-Meditation with OM
12-Boat	24-Final guided relaxation during corpse pose and OM chant (mantra traditionally chanted at the beginning and/or end of yoga sessions)

We hypothesized that BC patients enrolled in the 8-week BYP-BC will show decreased CRF compared to BC patients on the waiting list.

Materials and Methods

This study was approved by the ethical and scientific review board of the three participating hospitals in Montreal (Canada). Written informed consent was obtained from all participants. It was clearly stated that their approval or disapproval to participate in the study at any point in time would not interfere with their cancer treatments. To ensure confidentiality, alphanumeric codes were created to label their questionnaires. Consent forms and contact information were kept in a separate folder from their participants' folder.

Participants

Enrollment for the study occurred over a 2-year period from 2011 to 2013. Participants were recruited by nurses through direct contact during initial scheduled clinical visits. Eligibility was based on understanding French, being 18 years or older, having a BC diagnosis (stage I–III), receiving chemotherapy, having consent from one's medical team, having no regular practice of yoga, not currently undergoing psychotherapy and having no psychiatric diagnosis or heart failure. Eligibility was further confirmed by research assistants prior to study enrollment. The hospital staff enrolling participants was blinded to the allocation sequence. Group assignment was determined by a computer-generated random table in cohorts of 10 with an allocation ratio of 1:1. Blinding of participants and research assistants to group assignment was not possible due to the nature of the intervention. The treatment group received the BYP-BC for 8 weeks along with standard care. Concurrently, the wait-list (WL) control group only received standard care for 8 weeks followed by the BYP-BC for an additional 8 weeks.

Standard care consisted of psychoeducational information about BC treatments, side effects and available resources (support groups, counseling, and nutritionist), appointments with oncologists and follow-up appointments with nurses to assess symptom management, disease progression and treatment response.

The BYP-BC Intervention

The intervention consisted of eight weekly 90-minute group sessions, led by one instructor with five patients per group. Participants were also given a DVD of the intervention with a 20- and 40-minute session format. The sessions were held in each hospital's oncology department conference room. A standardized handbook detailing the BYP-BC weekly procedures was provided to yoga teachers.

The BYP-BC combines several relaxation periods between Hatha yoga poses, breathing techniques, visualization, and meditation. The main purpose of this program is to promote body and mind awareness and relaxation response. Each session followed the same format, namely an introduction of the psychoeducational theme (5 minutes), guided relaxation based on the theme (10 minutes), combination of gentle yoga poses and relaxation with breathing techniques (60 minutes), guided meditation with OM chant (7 minutes), and final relaxation (8 minutes). The eight psychoeducational themes were as follows: the importance and benefits of relaxation, the definition and causes of stress, the power of a concentrated mind and positive imagery, immune system function, activating the healing response, the benefits of breathing, acceptance philosophy, and the importance of daily yoga practice. During the session, the yoga instructor emphasized the importance of awareness of one's physical sensation and discussed the physiological and psychological benefits of each pose. In sum, 24 poses were included in the program and alternative poses adapted to the participants' conditions were also suggested. Participants were instructed to practice at home daily using the 20-minute session format for the first 4 weeks and the 40-minute session format for the four remaining weeks.

For a full description of the yoga poses and psychoeducational themes used in the study the first author can be contacted by email. Table 1 presents the list of poses.

Measures

The measurements were taken at baseline, 8, and 16 weeks. The outcomes were measured on the same time schedule for both groups, except at 16 weeks, at which time measurements were taken for the WL group exclusively. Medical and demographic information was obtained by using medical records and study-specific forms. Participants in the BYP-BC group were asked to record their home yoga practice in a diary, and for participants in the WL group, a daily diary of their activities during the waiting period and then during the yoga program.

CRF was assessed with the Multidimensional Fatigue Inventory (MFI-20)⁴⁴ which is a 20-item self-rated inventory. This inventory provides a profile of fatigue and is comprised of four domains: general fatigue (including physical fatigue, GPF) mental fatigue (MF), reduced activities (RA) and motivation (MOT). Participants had to use a 7-point scale (yes, that is true to no, that is not true) to rate the extent to which each statement applies to them. Higher scores indicate greater fatigue. Internal consistency for each subscale is: GPF (0.92), MF (0.84), RA (0.68) and MOT (0.73). Test re-test reliability is 0.83.

Analysis

Participants' clinical and sociodemographic characteristics and baseline MFI-20 scores were analyzed using univariate, correlation analyses and X ² tests to determine between group differences. An intent-to-treat analysis using ProcMixed Models was employed. Repeated measures analyses were conducted to assess within-group changes over time (baseline-8 weeks) and between-group differences (BYP-BC group vs. WL group) with regards to CRF. The P level was set at 0.05 for each analysis and each effect size was reported using the r coefficient. Primary outcome data were analyzed with Statistical Analysis System (SAS version 9.4) and descriptive statistics were conducted using Statistical Package for Social Sciences (SPSS version 22).

Results

Participants

Forty-eight patients were randomized and participated in the study. Ultimately, thirty-eight patients completed the study (Fig. 1). The only significant statistical differences between completers and non-completers were found on baseline muscle pain: 32% of participants reporting muscle pain failed to complete the study (P = 0.03) and chemotherapy: non-completers had less chemotherapy than their counterparts (2.81 ± 1.3 vs. 4.43 ± 1.5, P = 0.002). Due to the small sample size, possible confounding variables were not included such as chemotherapy cycles throughout 8 weeks, practice of physical activity or prescribed medication (Table 2). Lastly, class attendance for the BYP-BC group was 5.9 ± 2.7 sessions while participants practiced 1.4 ± 0.8 hours per week at home. No adverse effects were reported due to study intervention.

Figure 1.

Enrollment, patient flow of randomized clinical trial.

Table 2.

Sample Characteristics

Demographic and clinical characteristics	Total (n = 48)	Treatment/BYP-BC group (n = 25)	Control/WL (n = 23)	P
Age (years), mean (SD)	50.8 (8.3)	50.3 (1.7)	51.3 (1.7)	0.685
Race, n (%)
White	45 (95.7)	25 (100)	20 (91.3)	0.305
Nonwhite	3 (4.3)	0 (0)	3 (8.7)
Family status, n (%)
Single	6 (12.5)	4 (16)	2 (8.7)	0.602
Law partner/married	42 (87.5)	21 (84)	21 (91.3)
Education, highest degree completed^*, n (%)^a
High school graduate	14 (29.2)	7 (28)	7 (30.4)	0.692
Postsecondary training	6 (12.5)	2 (8)	4 (17.4)
College graduate	14 (29.2)	8 (32)	6 (26.1)
University graduate	13 (27.1)	8 (32)	5 (21.7)
Employment status, n (%)
Full time	18 (37.5)	8 (32.0)	10 (45)	0.330
Part-time	5 (10.4)	3 (12.0)	2 (9.1)
Disability	17 (14.6)	11 (44.0)	6 (23.2)
Retired	5 (10.4)	3 (12.0)	2 (9.1)
Homemaker	1 (2.1)°	0 (0.0)	1 (4.5)
Welfare/unemployment	2 (4.2)	0 (0.0)	2 (9.1)
Treatment center^b, n (%)
Center 1	6 (12.5)	4 (16)	2 (8.7)	0.591
Center 2	30 (62.5)	14 (56)	16 (69.6)
Center 3	12 (5)	7 (28)	10 (45)
Breast cancer stage, n (%)
I	16 (33.3)	6 (24)	10 (43.5)	0.618
II	29 (60.4)	18 (72)	11 (47.8)
III	3 (6.3)	1 (4)	2 (8.7)
Chemotherapy regimen^c, n (%)
AC, CMF	15 (31.3)	9 (36)	6 (26.1)	0.321
FEC, AC-T, TAC	33 (68.8)	16 (64)	17 (73.9)
Chemotherapy cycles, mean (SD)	4.06 (1.6)	4.40 (1.7)	3.70 (1.3)	0.126
Prescribed medication, n (%)
Antidepressants	8 (16.7)	3 (12)	5 (21.7)	0.293
Anxiolytics	3 (6.3)	2 (8)	1 (4.4)	0.658
Benzodiazepines	23 (47.9)	13 (52)	10 (43.5)	0.555

n = 47 for education variable.

Center 1 = Centre Hospitalier de l'université de Montréal. Center 2 = Centre Intégré de Cancérologie de Laval. Center 3 = Centre Intégré de Cancérologie de la Montérégie.

AC, cyclophosphamide-doxuribicin; AC-T/TAC, cyclophosphamide-doxuribicin and taxol/cyclophosphamide doxuribicin and taxotere; CMF, cyclophosphamide-methotrexate-fluorouracil; FEC, fluorouracil (5FU)-epirubicin-cyclophosphamide; SD, standard deviation.

Effect of Yoga on CRF

GPF dimension

The group main effect was not significant F (1, 45) = 0.03, P = 0.86, r = 0.03] while a significant difference was found for the time main effect highlighting change over time [F (1, 45) = 8.65, P = 0.01, r = 0.40]. There was a significant interaction effect [F (1, 45) = 5.28, P = 0.03, r = 0.32]. Within the BYP-BC group, there was no significant increase in general fatigue [T (45) = −0.44, P = 0.67, r = 0.07] whereas the increase in the WL group was markedly higher [T (45) = −3.86, P = 0.000, r = 0.50]. However, there was no significant difference between both groups after 8 weeks [T (45) = −0.95, P = 0.35, r = 0.14].

MF dimension

No time main effect [F (1, 45) = 0.09, P = 0.77, r = 0.04] nor group main effect [F (1, 45) = 0.29, P = 0.59, r = 0.08] were found to be statistically significant. There was a trend interaction effect [F (1, 45) = 2.98, P = 0.09, r = 0.25]. However, there was no statistically significant results found within each group BYP-BC [T (45) = 1.33, P = 0.19, r = 0.19] and WL [T (45) = −1.10, P = 0.28, r = 0.10].

RA dimension

No time main effect [F (1, 45) = 0.19, P = 0.66, r = 0.06], group main effect [F (1, 45) = 0.05, P = 0.82, r = 0.03] nor interaction effect [F (1, 45) = 0.07, P = 0.80, r = 0.04] were found to be statistically significant.

MOT dimension

No time main effect [F (1, 45) = 0.02, P = 0.89, r = 0.02] nor group main effect [F (1, 45) = 2.17, P = 0.15, r = 0.21] were found to be statistically significant. There was a significant interaction effect [F (1, 45) = 15.00, P = 0.00, r = 0.50]. Within the BYP-BC group, there was a statistically significant improvement in motivation [T (45) = 2.68, P = 0.01, r = 0.37] whereas it worsened in the WL group [T (45) = 2.79, P = 0.01, r = 0.24]. Lastly, a statistically significant difference was found between the BYP-BC and WL groups at 8 weeks [T (45) = 3.05, P = 0.00, r = 0.41]. The BYP-BC group had a lower reduced motivation score whereas the WL group had an increased reduced motivation score after 8 weeks (Table 3).

Table 3.

Mean Scale Scores and Standard Deviations of MFI-20 Subscale Scores

	BYP-BC				WL
	Pre (n = 25)		Post (n = 19)		Pre (n = 23)		Post (n = 19)
	M	SD	M	SD	M	SD	M	SD
GPF^*	41.78	10.47	43.03	9.64	37.21	8.86	45.22	9.47
MF	21.76	7.49	21.12	5.30	19.97	8.34	22.83	8.05
RA	11.41	3.58	11.08	3.93	11.04	4.86	10.97	4.72
MOT^*	7.58	2.85	6.44	2.06	7.12	2.18	8.60	3.07

P < 0.05.

GPF, general/physical subscale; MF, mental fatigue subscale; MOT, motivation subscale; Pre, baseline assessment; Post, assessment after 8 weeks; RA, reduced activities subscale.

Discussion

We hypothesized that BYP-BC would help reduce fatigue among BC patients undergoing chemotherapy. Conclusions drawn based on our results must be considered cautiously and considered preliminary results as few studies investigating the effects of yoga with a BC population receiving chemotherapy exclusively, have been conducted. Nevertheless, our findings partially confirmed our hypothesis. The significant interaction for the general and physical fatigue domain revealed that the WL group scores worsened from baseline to post-test compared to the BYP-BC group. It has been reported that gradual worsening of symptoms throughout cancer and its treatments can be expected.⁴⁵

More importantly, the large effect size found within this group (r = 0.50) would suggest this change to be of clinical significance. It could be speculated that the BYP-BC acts as a buffer and reduces the worsening of general-physical fatigue. Similar results have been found with the BYP-BC for depressive symptoms.⁴²

The yoga intervention did not seem to have a significant impact on the cognitive aspects of fatigue nor on improving reduced activities. Firstly, despite being a marginal trend, it is noteworthy to mention that the means obtained for the mental fatigue dimension follow a similar response pattern as the general-physical fatigue dimension across both groups. Secondly, the reduced activities dimension refers to the capacity of a patient to be able to do or not do something physically. It could be argued that participants' baseline for managing their different activities was not interrupted despite feeling fatigue and the BYP did not manage to improve that existing capacity. For example, several studies have highlighted the benefits of exercise in managing CRF.^6,10 It would be worthwhile to assess if and how participants' physical activity impact CRF's domains.

The most convincing results relate to the motivation subscale. Our findings revealed a significant interaction where the BYP-BC group showed a moderate improvement in motivation whereas the WL group seemed to worsen. Moreover, motivation is the only domain where both groups differed significantly after 8 weeks. This subscale refers to the difficulty or not of imagining a pleasant activity.⁴⁴ It is possible benefiting from BYP-BC is a self-care enjoyable activity, enabling patients to improve their mood and having something to look forward to despite feeling fatigued due to the toll of chemotherapy. Additional studies investigating possible links between fatigue, motivation and yoga interventions could be helpful.

Overall, our results do not fully corroborate other research findings concluding yoga's beneficial effect in reducing fatigue. However, several methodological differences merit to be highlighted. Firstly, it is possible less significant results were found due to the variability of adherence to yoga intervention and home practice (5.9 ± 2.7 sessions, 1.7 ± 0.8 hours per week for home practice). Most yoga interventions in the RCTs were either several times per week or longer in duration and adherence was highly rated.³² Therefore, a dose-response relationship could be argued and improving class attendance and home practice could be a starting point in evaluating the potential benefits of BYP-BC on mental fatigue and reduced activities.

This study has several limitations. Firstly, the small sample size, lack of power and attrition prevents us from making generalizable inferences and limiting the detection of meaningful statistical differences. Also, the significant difference found where non-completers suffered from muscle pain introduces bias which further limits the generalizability of the findings. Significant results could also be explained due to response bias of the experimental group reporting feeling better due to receiving BYP-BC as opposed to the control group not receiving an intervention. Several variables related to CRF were not assessed and could act as confounding variables such as sleep quality and/or disturbance and personality variables.⁴⁶ Moreover, patients' expectations and prior history related to fatigue was not assessed.

Despite its limitations, this study provided further evidence of yoga's potential benefits in reducing and/or managing CRF. Moreover, a multidimensional measure was used to capture the different domains of CRF. We also conducted several preliminary analyses to exclude possible confounding variables such as duration, frequency and type, cycles of chemotherapy, cancer stage and sociodemographic variables. Lastly, the study was conducted within a homogenous sample receiving chemotherapy exclusively and no injuries or adverse events were reported.

Conclusion

As yoga is becoming increasingly popular among BC patients, a better understanding of its clinical significance in managing the distressing symptom of CRF is paramount. Moreover, it has been well documented how CRF disrupts and decreases an individual's quality of life. Worst of all, CRF is said to remain problematic for one third of cancer survivors. It has also been established and recommended to maintain physical activity to promote well-being and survivorship. This study will add to the growing body of research pertaining to yoga and CRF.

However, it is important to reiterate these results are preliminary due to the small sample size. Therefore, additional RCTs with larger and homogenous sample sizes and improved assessments of CRF and its confounding variables need to be conducted to determine to what extent yoga can be a beneficial complementary adjunct in cancer support care.

Footnotes

Acknowledgments

The authors would like to thank Madan Bali, Maryse Carignan, MD, Sylvie Coallier, PhD, Sonia Joannette, and Jill Vandermeschen for their contribution. Support of this research was provided by the Centre de liaison sur l'intervention et la prevention psychosociale (CLIPP).

Author Disclosure Statement

No competing financial interests exist.

Funding Information▪

The authors received no financial support for this research.

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