Abstract
There is growing interest in understanding the influence of yoga on health outcomes and health-related quality of life among cancer survivors. This cross-sectional study evaluated the effects of participating in regular exercise alone or in conjunction with yoga on health-related quality of life among 219 ovarian cancer survivors using the SF-36 health survey. Multivariate regression was used to assess the association between the exercise/yoga categories on the 8 SF-36 scales. The results suggest that survivors who participated in both regular exercise and yoga had higher scores in physical functioning, fewer limitations with physical and emotional health, less pain, and more vitality than survivors who reported participating in regular exercise only. These results highlight the utility of exercise as a potential predictor of health-related quality of life in ovarian cancer survivors and support adding yoga to an exercise program.
Introduction
It is estimated that approximately 22 000 women in the United States were diagnosed with ovarian cancer in 2010. 1 For such women, changes in health-related quality of life associated with their diagnosis can be substantial, and they may experience depression and anxiety. 2 The majority of women who are diagnosed with ovarian cancer will be treated with cytoreductive surgery and primary postoperative chemotherapy. These treatment modalities can also have a considerable influence on health-related quality of life and can result in physical symptoms such as nausea/vomiting, peripheral neuropathy, alopecia, fatigue, loss of cognitive function, and sexual dysfunction. 2 Learning to manage the emotional sequelae associated with an ovarian cancer diagnosis and the symptoms that are commonly experienced with treatment is a challenging task for both patients and their oncologists.
Exercise has long been known to have a positive effect on overall health outcomes and health-related quality of life in cancer patients, and there is currently growing interest in understanding the influence of yoga on overall health outcomes and health-related quality of life among cancer survivors. Yoga is a gentle form of exercise that focuses on improving strength and flexibility while fostering peace through mindful movement and breathing. A randomized trial of 88 breast cancer patients reported that patients who participated in a 6-week yoga program had statistically significantly lower levels of anxiety, depression, perceived stress, and cortisol levels than those who received 6 weeks of support therapy. 3 Results from this trial also showed that patients who were randomized to the yoga intervention also had higher positive affect, higher emotional and cognitive functioning, and lower negative affect than patients who received support therapy. 4 Another randomized trial of breast cancer patients reported a statistically significant decrease in the frequency of post-chemotherapy-induced nausea, nausea intensity, anticipatory nausea, and anticipatory vomiting in the patients who were randomized to participate in yoga compared with those who received supportive therapy. 5
Despite these positive findings, there has been limited research conducted on the influence of yoga on ovarian cancer survivors. To our knowledge, no studies of ovarian cancer survivors have evaluated whether adding yoga to an existing exercise program would enhance health-related quality of life beyond what is observed by the exercise program alone. Therefore, using ovarian cancer survivors who did not participate in regular exercise or yoga as the reference group, we sought to test the hypothesis that ovarian cancer survivors who reported participating in regular exercise and yoga had statistically significantly higher levels of health-related quality of life than ovarian cancer survivors who reported participating in regular exercise alone.
Methods
Study Population
Potential study participants were identified through 2 gynecological oncology offices. Ovarian cancer survivors were considered eligible for this cross-sectional study if they spoke fluent English and were older than 21 years. Based on these criteria, 447 women were deemed eligible to participate. Of the 447 women who were eligible to participate in the study, a current mailing address was available for 388 (87%) survivors. These women were informed about the study via a mailing from the gynecological oncology office that provided treatment for their cancer. The mailing included a letter with detailed information about the study, 2 copies of the informed consent, and a questionnaire. In addition, a self-addressed postage-paid envelope was provided in the packet to ensure the study materials could be returned at no cost to the participant. Follow-up telephone calls were made by study personnel to each ovarian cancer survivor who received a packet but did not respond to the mailing.
Study Measures
The study questionnaire included questions related to demographics, conventional treatment for ovarian cancer (ie, surgery and type of chemotherapy), current or follow-up conventional treatment, symptoms associated with conventional treatment, use of complementary and alternative medicine (CAM) providers (ie, naturopaths, massage therapists, and chiropractors), use of herbs or supplements, participation in CAM activities (ie, yoga, exercise, mediation, biofeedback, journaling, and mental imagery), and functional health status using the SF-36. Questions related to CAM activities were structured as, “Since your diagnosis with ovarian cancer, have you participated in any of the following activities?” The study participant could respond “yes” or “no.” If they responded “yes,” they were then asked if the activity was helpful and could respond “yes,” “no,” or “don’t know.”
Assessment of Health-Related Quality of Life
Health-related quality of life was assessed using the SF-36 health survey. This is a commonly used and well-validated tool for measuring mental and physical well-being. It quantifies the health-related quality of life of patients using 8 scales: physical functioning, limitations associated with physical health, limitations associated with emotional problems, vitality, emotional well-being, social functioning, pain, and general health. The scales are scored from 0 to 100 using weighted sums of the questions in each section, with 100 indicating the highest level of functioning and the best quality of life.
Statistical Analysis
Women were categorized into 3 groups based on their self-reported participation in regular exercise and/or yoga: no exercise or yoga (n = 93, 42.5%), regular exercise only (n = 98, 44.7%), and both regular exercise and yoga (n = 28, 12.8%). Descriptive statistics (including means and standard deviations for continuous variables and frequencies and percentages for categorical variables) were used to summarize the characteristics of the study sample, side effects associated with chemotherapy, and participant perceptions regarding CAM activities among women in each of the 3 exercise/yoga categories. Fisher’s exact test was used to test the null hypothesis that there were no differences between the demographic variables or the chemotherapy-related side effects across the 3 exercise and yoga groups. Using the nonexercisers as the referent group, multivariate linear regression was used to assess the association between each exercise category and the 8 SF-36 scales, adjusting for factors that are known to be associated with health-related quality of life (ie, stage at diagnosis, years since diagnosis, age, and education). One model was built for each of the 8 SF-36 scales.
Results
Completed questionnaires were returned by 219 of the 388 survivors who had been invited to participate in the study. This equates to a response rate of 56.4%. Table 1 summarizes the patient characteristics of the study sample. There was a statistically significant difference in the mean age of the study participants across the 3 exercise groups (P=0.007). The majority of the total sample was white (86%), had completed college (37%), were diagnosed with ovarian cancer 2 to 5 years ago (37%), were diagnosed with stage III disease (51%), were treated with surgery and chemotherapy (88%), and had not had a recurrence at the time of the survey (55%). There was a statistically significant association between level of education and the 3 exercise/yoga groups (P = .02). Specifically, higher levels of education tended to equate to a higher participation in exercise or yoga. Of the 30 survivors who reported obtaining a high school diploma or GED, 60% reported no exercise or yoga, 37% reported regular exercise only, and 3% reported regular exercise and yoga. Conversely, of the 81 survivors who reported completing college, 36% reported no exercise or yoga, 44% reported regular exercise only, and 20% reported regular exercise and yoga. Approximately 37% of the sample experienced recurrence, and the mean time to recurrence was 24 months.
Patient Characteristics
Abbreviation: SD, standard deviation.
aPercentages were calculated using row totals.
Table 2 describes the side effects that lasted more than 6 months among the 200 survivors that reported having chemotherapy following their treatment. The most commonly reported side effect was neuropathy, which was experienced by 58% of the survivors. There was a statistically significant difference in the proportion of survivors who reported experiencing neuropathy following chemotherapy across the exercise and yoga groups. Specifically, neuropathy was experienced by 49% of the survivors who reported no exercise or yoga, 41% of the survivors who reported regular exercise only, and 9% of the survivors who reported regular exercise and yoga (P = .05). There was also a statistically significant difference in the proportion of survivors who reported experiencing pain (bone/muscle) following chemotherapy across the exercise and yoga groups. Approximately 20% of the total sample, 59% of the survivors who reported engaging in no exercise or yoga, 36% who reported engaging in regular exercise only, and 5% who reported engaging in regular exercise and yoga (P = .05) experienced bone or muscle pain.
Side Effects That Lasted More Than 6 Months Following Chemotherapy Among Ovarian Cancer Survivors
aPercentages were calculated as column totals.
bPercentages were calculated as row totals
Table 3 summarizes the health-related quality-of-life outcomes as measured by the 8 subscales of the SF-36. The scales are scored from 0 to 100, with 100 indicating the highest level of functioning and the best quality of life. Using the nonexercisers as the reference group, survivors who reported participating in both regular exercise and yoga tended to have higher scores on measures of physical functioning than survivors who reported only participating in regular exercise (β = 19.67, P < .001; β = 11.21, P < .001, respectively). Survivors who participated in regular exercise and yoga also reported fewer limitations associated with physical health (β = 27.29, P = .006; β = 10.25, P = .112, respectively), fewer limitations associated with emotional health (β = 22.04, P = .007; β = 13.69, P = .012, respectively), less pain (β = 9.83, P = .051; β = 7.94, P = .018, respectively), and more vitality (β = 12.08, P = .021; β = 11.81, P = .001, respectively). The 2 exercise groups had similar scores for social functioning (β = 11.32, P = .019; β = 12.05, P = .001, respectively). Conversely, survivors who reported participating in both regular exercise and yoga tended to have higher scores on measures of general health than survivors who reported participating only in regular exercise (β = 9.83, P = .033; β = 11.84, P = .001). A similar pattern was also observed for measures of emotional well-being; however, these associations were not statistically significant (β = −3.66, P = .340; β = −0.44, P = .860, respectively).
Multiple Regression Results (Adjusting for Stage at Diagnosis, Years Since Diagnosis, Age, Education, Bone Pain, and Neuropathy)
aReference group: survivors who reported no exercise or yoga.
The percentage of survivors who engaged in a CAM activity and found it to be helpful is summarized in Table 4. A total of 55% of the sample reported engaging in regular exercise, and 95% of those survivors felt that exercise was helpful. Only 12% of the sample reported practicing yoga; however, 89% of those survivors felt that it was helpful. Other CAM activities that were perceived as being helpful included practicing meditation (21% participated, 96% found it to be helpful), using mental imagery (18% participated, 90% found it to be helpful), and using homeopathic preparations (6% participated, 100% found it to be helpful). A non-CAM activity that also was perceived as being helpful included using prayer (50% participated, 95% found it to be helpful).
Percentage of Ovarian Cancer Survivors (n=219) that Did Extra Activity and Found It to Be Helpful
aPercentages were calculated as column totals.
bPercentages were calculated as row totals.
Discussion
Epidemiological and clinical studies have shown that weight gain after a cancer diagnosis is associated with an increased risk of recurrence and mortality 6 and that participating in an exercise program results in improved physical functioning, strength, physical activity levels, overall quality of life, fatigue, immune function, and hemoglobin levels. 7 Despite these positive findings, beginning or maintaining an exercise program following a cancer diagnosis can be challenging. It has been reported that a small proportion of ovarian cancer survivors are participating in regular exercise following their cancer diagnosis. For example, a survey of 359 ovarian cancer survivors in Canada found that only one third were meeting the public health physical activity guidelines, which include 60 minutes of strenuous or 150 minutes of moderate or strenuous physical activity per week. 8 This is far lower than what is observed among the 46% of women 45 to 64 years of age and 36% of women who are 65 years or older in the general population who meet the current physical activity guidelines. 9 It has also been reported that almost 40% of ovarian cancer survivors decreased their physical activity during the first year after their diagnosis, 24% of the survivors reported decreased activity 2 to 3 years after diagnosis, and 28% reported decreased activity ≥ 4 years after diagnosis. 10 Despite these findings, there is evidence to suggest that more than half of ovarian cancer survivors are interested in participating in an exercise program. 11 The challenge for patients and clinicians may be finding an activity that is both acceptable and beneficial to the patients.
Many forms of yoga are not strenuous and are likely to be a good exercise choice for cancer survivors throughout their treatment, into remission, and beyond. A review of studies on yoga among cancer survivors found that yoga was well tolerated by cancer patients and that adherence rates to yoga programs were generally high. 12 In addition, it was found that the gentle yoga poses, which involve stretching and deep breathing, were successfully performed by survivors with a wide range of physical limitations. 12 These poses are likely to be an ideal exercise choice for patients who are coping with the physical symptoms associated with ovarian cancer treatment, such as nausea/vomiting, peripheral neuropathy, fatigue, and loss of cognitive function.
Unfortunately, there has been very little research on the association between yoga and health-related quality of life among ovarian cancer survivors. To our knowledge, only 1 small pilot study has reported results on this topic. 13 In this study, 37 ovarian cancer patients and 14 breast cancer patients participated in 10 weekly, 75-minute restorative yoga classes. The objective of this study was to assess the feasibility of implementing a yoga program for women who had been diagnosed with ovarian or breast cancer and to evaluate changes in fatigue, psychological distress and well-being, and quality of life at baseline, immediately after completing the series of yoga classes, and 2 months after completing the series of yoga classes. Qualitative results of this study indicated that women felt positive about the relaxation that occurred during the classes and the overall group experience. Quantitative results indicated improvements in depression, anxiety, and overall quality of life. In addition, symptoms of fatigue were reported to be improved between baseline and immediately after completing the series of yoga classes. Finally, this study reported that health-related quality of life improved between baseline and the 2-month follow-up.
The results of our study suggest that survivors who participated in both regular exercise and yoga had higher scores in physical functioning, fewer limitations with physical and emotional health, less pain, and more vitality than survivors who reported participating in regular exercise only. In addition, 95% of the survivors who participated in exercise found it to be helpful. The same was true for 89% of the survivors who participated in yoga. The temporal inferences that can be drawn from these results are limited due to the cross-sectional design of our study. In addition, our survey did not include questions regarding the frequency, duration, or type of exercise or yoga in which each survivor participated. As such, we were unable to evaluate if these factors had a differential influence on the observed health-related quality of life. However, our results do provide a foundation for future work in this area. There is clearly a need for more studies that are designed to evaluate the influence of yoga on health-related quality of life among ovarian cancer survivors. Surgical and medicinal treatments for this disease are advancing, which has fortunately led to improvements in overall survival. As of January 1, 2008, it was found that 177 578 women in the United States had been diagnosed with ovarian cancer and were still alive. 14 This may lead ovarian cancer to be classified as a “chronic cancer,” 2 for which creative measures for enhancing health-related quality of life must be used.
Footnotes
Author Contributions
MRA, LS, and ES designed and implemented the study. BAG and CWD provided oversight to the study design. BAG and CWD are gynecological oncologists, and the study participants were recruited from their practices. KAL conducted the statistical analyses in this study and wrote this article. All authors provided comments to the manuscript and approved the final version of the manuscript.
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This collaborative work was supported by funding from the Rivkin Cancer for Ovarian Cancer Research.
Ethical Approval
Study methods and the questionnaires used for this research were reviewed and approved by the institutional review board of the Fred Hutchinson Cancer Research Center.