Advertisement

Yoga for Women with Metastatic Breast Cancer: Results from a Pilot Study

  • James W. Carson
    Correspondence
    Address reprint requests to: James W. Carson, PhD, Pain Prevention & Treatment Research Program, Department of Psychiatry, Duke University Medical Center, Box 90399, Durham, NC 27708, USA.
    Affiliations
    Departments of Psychiatry and Behavioral Sciences (J.W.C., K.M.C., L.S.P., F.J.K., J.M.M.) and Medicine (H.S.), Duke University Medical Center, Durham, North Carolina, USA
    Search for articles by this author
  • Kimberly M. Carson
    Affiliations
    Departments of Psychiatry and Behavioral Sciences (J.W.C., K.M.C., L.S.P., F.J.K., J.M.M.) and Medicine (H.S.), Duke University Medical Center, Durham, North Carolina, USA
    Search for articles by this author
  • Laura S. Porter
    Affiliations
    Departments of Psychiatry and Behavioral Sciences (J.W.C., K.M.C., L.S.P., F.J.K., J.M.M.) and Medicine (H.S.), Duke University Medical Center, Durham, North Carolina, USA
    Search for articles by this author
  • Francis J. Keefe
    Affiliations
    Departments of Psychiatry and Behavioral Sciences (J.W.C., K.M.C., L.S.P., F.J.K., J.M.M.) and Medicine (H.S.), Duke University Medical Center, Durham, North Carolina, USA
    Search for articles by this author
  • Heather Shaw
    Affiliations
    Departments of Psychiatry and Behavioral Sciences (J.W.C., K.M.C., L.S.P., F.J.K., J.M.M.) and Medicine (H.S.), Duke University Medical Center, Durham, North Carolina, USA
    Search for articles by this author
  • Julie M. Miller
    Affiliations
    Departments of Psychiatry and Behavioral Sciences (J.W.C., K.M.C., L.S.P., F.J.K., J.M.M.) and Medicine (H.S.), Duke University Medical Center, Durham, North Carolina, USA
    Search for articles by this author

      Abstract

      Metastatic breast cancer (MBC) remains a terminal illness for which major treatment advances are slow to appear, and hence it is crucial that effective palliative interventions be developed to reduce the cancer-related symptoms of women with this condition during the remaining years of their lives. This pilot/feasibility study examined a novel, yoga-based palliative intervention, the Yoga of Awareness Program, in a sample of women with MBC. The eight-week protocol included gentle yoga postures, breathing exercises, meditation, didactic presentations, and group interchange. Outcome was assessed using daily measures of pain, fatigue, distress, invigoration, acceptance, and relaxation during two preintervention weeks and the final two weeks of the intervention. Thirteen women completed the intervention (mean age=59; mean time since diagnosis=7 years; two African American, 11 Caucasian). During the study, four participants had cancer recurrences, and the physical condition of several others deteriorated noticeably. Despite low statistical power, pre-to-post multilevel outcomes analyses showed significant increases in invigoration and acceptance. Lagged analyses of length of home yoga practice (controlling for individual mean practice time and outcome levels on the lagged days) showed that on the day after a day during which women practiced more, they experienced significantly lower levels of pain and fatigue, and higher levels of invigoration, acceptance, and relaxation. These findings support the need for further investigation of the effects of the Yoga of Awareness Program in women with MBC.

      Key Words

      Introduction

      Metastatic breast cancer (MBC) constitutes a serious life threat for women, with an average prognosis of 18–24 months to live.
      • Leonard R.C.
      • Rodger A.
      • Dixon J.M.
      • Dixon J.M.
      Metastatic breast cancer.
      Pain, fatigue, and emotional distress are often reported as the most debilitating symptoms of MBC patients.
      • Aranda S.
      • Schofield P.
      • Weih L.
      • et al.
      Mapping the quality of life and unmet needs of urban women with metastatic breast cancer.
      • Cella D.
      Factors influencing quality of life in cancer patients: anemia and fatigue.
      • Patrick D.L.
      • Ferketich S.L.
      • Frame P.S.
      • et al.
      National Institutes of Health State-of-the-science conference statement: symptom management in cancer: pain, depression, and fatigue.
      • Rowland J.H.
      • Massie M.J.
      • Holland J.C.
      Breast cancer.
      Although pharmacological interventions may help these women to some degree, these symptoms rarely resolve.
      • Patrick D.L.
      • Ferketich S.L.
      • Frame P.S.
      • et al.
      National Institutes of Health State-of-the-science conference statement: symptom management in cancer: pain, depression, and fatigue.
      • Foley K.M.
      • Arbit E.
      • DeVita V.T.
      • Hellman S.
      • Rosenberg S.A.
      Management of cancer pain.
      • Osoba D.
      • Slamon D.J.
      • Burchmore M.
      • et al.
      Effects on quality of life of combined trastuzumab and chemotherapy in women with metastatic breast cancer.
      Given that MBC is a terminal illness for which major treatment advances are slow to appear, it is crucial that effective adjunctive palliative interventions be developed to reduce the cancer-related symptoms of these women during the remaining years of their lives.
      Few palliative behavioral interventions have been tested with MBC patients, with mixed results. A recent review of cognitive-behavioral group therapy
      • Cunningham A.J.
      • Edmonds C.V.
      • Jenkins G.P.
      • et al.
      A randomized controlled trial of the effects of group psychological therapy on survival in women with metastatic breast cancer.
      • Edelman S.
      • Bell D.R.
      • Kidman A.D.
      A group cognitive behaviour therapy programme with metastatic breast cancer patients.
      • Edelman S.
      • Lemon J.
      • Bell D.R.
      • Kidman A.D.
      Effects of group CBT on the survival time of patients with metastatic breast cancer.
      • Edmonds C.V.
      • Lockwood G.A.
      • Cunningham A.J.
      Psychological response to long-term group therapy: a randomized trial with metastatic breast cancer patients.
      and supportive-expressive group therapy
      • Bordeleau L.
      • Szalai J.P.
      • Ennis M.
      • et al.
      Quality of life in a randomized trial of group psychosocial support in metastatic breast cancer: overall effects of the intervention and an exploration of missing data.
      • Classen C.
      • Butler L.D.
      • Koopman C.
      • et al.
      Supportive-expressive group therapy and distress in patients with metastatic breast cancer: a randomized clinical intervention trial.
      • Goodwin P.J.
      • Leszcz M.
      • Ennis M.
      • et al.
      The effect of group psychosocial support on survival in metastatic breast cancer.
      • Spiegel D.
      • Bloom J.R.
      • Yalom I.
      Group support for patients with metastatic cancer.
      • Spiegel D.
      • Bloom J.R.
      Group therapy and hypnosis reduce metastatic breast carcinoma pain.
      • Spiegel D.
      • Bloom J.R.
      • Kraemer H.C.
      • Gottheil E.
      Effect of psychosocial treatment on survival of patients with metastatic breast cancer.
      trials concluded that although some evidence exists for short-term benefits from these approaches (e.g., better mood
      • Edelman S.
      • Bell D.R.
      • Kidman A.D.
      A group cognitive behaviour therapy programme with metastatic breast cancer patients.
      • Spiegel D.
      • Bloom J.R.
      • Yalom I.
      Group support for patients with metastatic cancer.
      and less increase in pain
      • Goodwin P.J.
      • Leszcz M.
      • Ennis M.
      • et al.
      The effect of group psychosocial support on survival in metastatic breast cancer.
      • Spiegel D.
      • Bloom J.R.
      Group therapy and hypnosis reduce metastatic breast carcinoma pain.
      ), such changes are not maintained even for a few months.
      • Edwards A.G.
      • Hailey S.
      • Maxwell M.
      Psychological interventions for women with metastatic breast cancer.
      More recently, results from an exercise intervention tailored for MBC demonstrated short-term effects in terms of slower rates of deterioration in well-being and fatigue.
      • Headley J.A.
      • Ownby K.K.
      • John L.D.
      The effect of seated exercise on fatigue and quality of life in women with advanced breast cancer.
      There is thus a clear need to test new behavioral approaches to ameliorating cancer-related symptoms in women with MBC.
      • Edwards A.G.
      • Hailey S.
      • Maxwell M.
      Psychological interventions for women with metastatic breast cancer.
      Yoga is a popular approach to health maintenance, which holds promise for benefiting women with MBC. As a mind/body discipline originating in India, yoga has been practiced for its proposed physical, mental, and spiritual benefits for thousands of years.
      • Telles S.
      • Naveen K.V.
      Yoga for rehabilitation: an overview.
      Yoga is one of a variety of complementary and alternative medicine adjunctive approaches that cancer patients of all cultural backgrounds have been seeking out in dramatically larger numbers in recent years.

      Alferi SM, Antoni MH, Ironson G, Kilbourn KM, Carver CS. Factors predicting the use of complementary therapies in a multi-ethnic sample of early-stage breast cancer patients. J Am Med Womens Assoc. 2001;56:120–123.

      • Eisenberg D.M.
      • Davis R.B.
      • Ettner S.L.
      • et al.
      Trends in alternative medicine use in the United States, 1990–1997: results of a follow-up national survey.
      • Lee M.M.
      • Lin S.S.
      • Wrensch M.R.
      • Adler S.R.
      • Eisenberg D.
      Alternative therapies used by women with breast cancer in four ethnic populations.
      • Richardson M.A.
      • Sanders T.
      • Palmer J.L.
      • Greisinger A.
      • Singletary S.E.
      Complementary/alternative medicine use in a comprehensive cancer center and the implications for oncology.
      Yoga is now offered at several major treatment centers (e.g., M.D. Anderson, Memorial Sloan-Kettering, UCLA/Jonsson) via their complementary therapy services, and recently yoga has been the focus of several cancer studies.
      • Bower J.E.
      • Woolery A.
      • Sternlieb B.
      • Garet D.
      Yoga for cancer patients and survivors.
      • Brawley L.R.
      • Culos-Reed S.N.
      • Angove J.
      • Hoffman-Goetz L.
      Understanding the barriers to physical activity for cancer patients: review and recommendations.
      • Cohen L.
      • Warneke C.
      • Fouladi R.T.
      • Rodriguez M.A.
      • Chaoul-Reich A.
      Psychological adjustment and sleep quality in a randomized controlled trial of the effects of a Tibetan yoga intervention in patients with lymphoma.
      • Culos-Reed S.N.
      • Carlson L.E.
      • Daroux L.M.
      • Hately-Aldous S.
      A pilot study of yoga for breast cancer survivors: physical and psychological benefits.
      • Joseph C.D.
      Psychological supportive therapy for cancer patients.
      Results from two randomized trials of yoga for cancer patients have been published. Cohen et al. reported improvement in sleep disturbance in a trial with lymphoma patients,
      • Cohen L.
      • Warneke C.
      • Fouladi R.T.
      • Rodriguez M.A.
      • Chaoul-Reich A.
      Psychological adjustment and sleep quality in a randomized controlled trial of the effects of a Tibetan yoga intervention in patients with lymphoma.
      and Culos-Reed et al. demonstrated improvements in mood, quality of life, and stress in breast cancer survivors.
      • Culos-Reed S.N.
      • Carlson L.E.
      • Daroux L.M.
      • Hately-Aldous S.
      A pilot study of yoga for breast cancer survivors: physical and psychological benefits.
      However, thus far no study has investigated the use of yoga with MBC patients. The rationale for applying a yoga-based intervention in this population rests on several premises. First, research suggests that yoga can produce an “invigorating effect on mental and physical energy” that improves physical fitness and counteracts fatigue,
      • Wood C.
      Mood change and perceptions of vitality: a comparison of the effects of relaxation, visualization and yoga.
      a problematic symptom in MBC. Second, historically in the practice of yoga, a fundamental emphasis is placed on accepting one's moment-to-moment experiences, whatever they may be, without forcing the body beyond its comfortable limits. This is because struggles to control the body, or to control one's physical sensations, thoughts, or emotions often only exacerbate problems. Such struggles also detract from focusing on the personally fulfilling activities at hand. The important role of a healthy sense of acceptance in decreasing distress in the face of unpleasant symptomology has received increased research and clinical attention,
      • McCracken L.M.
      • Carson J.W.
      • Eccleston C.
      • Keefe F.J.
      Acceptance and change in the context of chronic pain.
      and may be especially important for individuals dealing with a life-threatening illness.
      • Clark D.
      Between hope and acceptance: the medicalisation of dying.
      Third, studies have demonstrated that yoga produces the relaxation response characterized by decreased sympathetic and increased parasympathetic activity.
      • Kamei T.
      • Toriumi Y.
      • Kimura H.
      • et al.
      Decrease in serum cortisol during yoga exercise is correlated with alpha wave activation.
      • Patel C.
      • North W.R.
      Randomised controlled trial of yoga and bio-feedback in management of hypertension.
      • Raghuraj R.
      • Telles S.
      Effect of a yoga-based and forced uninostril breathing on the autonomic nervous system.
      • Schell F.J.
      • Allolio B.
      • Schonecke O.W.
      Physiological and psychological effects of Hatha-Yoga exercise in healthy women.
      • Telles S.
      • Reddy S.K.
      • Nagendra H.R.
      Oxygen consumption and respiration following two yoga relaxation techniques.
      • Telles S.
      • Joshi M.
      • Dash M.
      • et al.
      An evaluation of the ability to voluntarily reduce the heart rate after a month of yoga practice.
      The relaxation response is likely to improve symptoms of pain, fatigue, and distress.
      • Lehrer P.M.
      • Woolfolk R.L.
      Principles and practice of stress management.
      • Nespor K.
      Pain management and yoga.
      In summary, yoga appears to promote at least three therapeutic processes—invigoration, acceptance, and relaxation—which are likely to have a favorable effect on MBC patients. The purposes of this pilot study were to determine the feasibility of a novel, yoga-based eight-week group intervention in women with MBC and to examine the intervention's effects on pain, fatigue, distress, invigoration, acceptance, and relaxation. We did not specify a priori hypotheses regarding improvements in these outcomes because of (a) the preliminary, uncontrolled design of the study and (b) the fact that significant findings from intervention studies with this population have often consisted of less deterioration in the intervention vs. control conditions, rather than actual improvement in symptoms.
      • Bordeleau L.
      • Szalai J.P.
      • Ennis M.
      • et al.
      Quality of life in a randomized trial of group psychosocial support in metastatic breast cancer: overall effects of the intervention and an exploration of missing data.
      • Goodwin P.J.
      • Leszcz M.
      • Ennis M.
      • et al.
      The effect of group psychosocial support on survival in metastatic breast cancer.
      • Spiegel D.
      • Bloom J.R.
      Group therapy and hypnosis reduce metastatic breast carcinoma pain.
      • Spiegel D.
      • Bloom J.R.
      • Kraemer H.C.
      • Gottheil E.
      Effect of psychosocial treatment on survival of patients with metastatic breast cancer.
      • Headley J.A.
      • Ownby K.K.
      • John L.D.
      The effect of seated exercise on fatigue and quality of life in women with advanced breast cancer.
      The intervention we used—the Yoga of Awareness Program—was specifically designed for MBC patients, and included gentle yoga postures, regulated breathing, guided meditations, brief didactic presentations, and group discussions.
      Compared to previous MBC intervention studies, this study makes a unique contribution in terms of the method of analyzing treatment outcome. Data on symptoms (pain, fatigue, distress) and therapeutic processes (invigoration, acceptance, relaxation) were collected in the form of prospective daily diaries. Relative to traditional survey questionnaires, diaries offer improved accuracy, reduced recall bias, and increased recall of symptoms and related events, especially regarding the temporal sequencing of events.
      • Carson J.W.
      • Keefe F.J.
      • Lynch T.R.
      • et al.
      Loving-kindness meditation for chronic low back pain: results from a pilot trial.

      Carson JW, Keefe FJ, Affleck G, et al. A comparison of conventional pain coping skills training and pain coping skills training with a maintenance training component: a daily diary analysis of short- and long-term treatment effects. J Pain 2006;7:615–625.

      • Stone A.A.
      • Kessler R.C.
      • Haythornthwaite J.A.
      Measuring daily events and experiences: decisions for the researcher.
      • Verbrugge L.M.
      Health diaries.
      • Bolger N.
      • Davis A.
      • Rafaeli E.
      Diary methods: capturing life as it is lived.
      To analyze the diary data, we used multilevel random effects models.
      • Affleck G.
      • Zautra A.
      • Tennen H.
      • Armeli S.
      Multilevel daily process designs for consulting and clinical psychology: a preface for the perplexed.
      These analyses are preferable to data analytic strategies that aggregate daily assessments (e.g., ordinary regression models) because they permit 1) tracking of symptom-related processes as they occur in naturalistic settings, 2) accounting for two levels of sampling, that is, both within-person variation and between-person variation, 3) controlling for autocorrelation, that is, the serial dependency that results from successive daily assessments, and 4) handling missing data that often occur in intensive longitudinal data collection.
      • Affleck G.
      • Zautra A.
      • Tennen H.
      • Armeli S.
      Multilevel daily process designs for consulting and clinical psychology: a preface for the perplexed.
      • Jaccard J.
      • Wan C.K.
      Statistical analysis of temporal data with many observations: issues for behavioral medicine data.
      • Schwartz J.E.
      • Stone A.A.
      Strategies for analyzing ecological momentary assessment data.
      • West S.G.
      • Hepworth J.T.
      Statistical issues in the study of temporal data: daily experiences.

      Methods

      Participants and Setting

      Volunteers for this study included 21 adult women with MBC referred by oncologists at the Duke University Medical Center breast oncology unit and affiliate sites. Sample illustrations of the postures used during the yoga sessions were provided to referring physicians and to potential participants to give them a better sense of what the intervention would involve. Patients were excluded if they had less than six-month life expectancy, if changes had taken place in their use of any antidepressants during the previous three months, if they had received treatment for serious psychiatric disorders (e.g., schizophrenia) in the previous six months, if they were currently engaged in intensive yoga practice (>three days per week), if driving time to attend weekly sessions was excessive (>one hour as a rule of thumb), or if they were not English speaking. Of the women who volunteered for the study, three withdrew before beginning the intervention (2=scheduling difficulties, 1=custody-case court appearances). Of the 18 remaining women, four withdrew shortly after beginning the intervention (1=scheduling difficulties, 1=traveling distance, 1=relocated to another state, 1=health status deterioration), and one woman did not complete post diaries because of mental status deterioration (dementia-like). Attrition subsequent to beginning the intervention was thus 28%, which is similar to other intervention studies with MBC patients (e.g., Edelman et al.
      • Edelman S.
      • Bell D.R.
      • Kidman A.D.
      A group cognitive behaviour therapy programme with metastatic breast cancer patients.
      =26%, Goodwin et al.
      • Goodwin P.J.
      • Leszcz M.
      • Ennis M.
      • et al.
      The effect of group psychosocial support on survival in metastatic breast cancer.
      =32%, Spiegel and Bloom=31%
      • Spiegel D.
      • Bloom J.R.
      Group therapy and hypnosis reduce metastatic breast carcinoma pain.
      ).
      This left 13 women who completed the intervention and provided pre- and postmeasures. The mean age of this sample was 59 years (range=44–75). The average time since diagnosis was seven years (range=0–26). Seven were concurrently receiving chemotherapy treatments, and six were not; four had new cancer reoccurrences while participating in the study. Six patients previously practiced yoga or meditation to some extent (of which two had practiced during the previous year). Eleven patients were Caucasian and two were African American. Eleven were married, one was widowed, and one was divorced. Fifteen percent had graduated from high school, 54% had attended college, and 31% had attended graduate school.

      Procedure

      The protocol for this study was approved by the Duke Institutional Review Board. Prior to the study, informed consent was obtained from all participants. All women were asked to provide basic demographic information and information relevant to their breast cancer treatment history. Participants continued to receive the standard care provided by their health care providers. To control for a potentially important medication-related confound, after completing the intervention, patients were asked about any changes in antidepressant use; no changes were reported. After completing the yoga program and postintervention measures, women were invited to participate in a focus group to give qualitative feedback regarding the program.

      Data Collection

      Daily Symptom and Process Measures

      A brief daily-diary measurement strategy was chosen because of the demonstrated reliability and validity of this method in health-related fields, and the fact that diaries allow subjective events, such as sensations and feelings, to be reported unobtrusively and with little introspection in individuals' natural settings.
      • Bolger N.
      • Davis A.
      • Rafaeli E.
      Diary methods: capturing life as it is lived.
      Data from diaries also permit a careful analysis of day-to-day interrelated happenings for each person and provide increased statistical power when analyzing a small clinical sample.
      • Schwartz J.E.
      • Stone A.A.
      Strategies for analyzing ecological momentary assessment data.
      Before going to bed each evening, patients completed a daily-diary log, in which they recorded their levels of pain, fatigue, distress, invigoration, acceptance, and relaxation during two preintervention weeks (pre), and during the last two weeks of the intervention period (post). All daily variables were indicated by marking 100-mm visual analogue scales (VAS), in which higher scores reflected greater amounts (e.g., for pain, the item read “Please indicate the average level of pain you had today,” with anchors set as “No Pain” and “Pain as Bad as it Can Be”; for acceptance, the item read “Please indicate how easy it was for you today to accept and let be the ways you have been affected by your medical condition,” with anchors set as “No Acceptance” and “Complete Acceptance”). Similar VAS measures are extensively used in clinical settings to measure subjective phenomena, and have been shown to be valid, reliable, rapid, and sensitive in measuring such variables as global affect, pain, and fatigue.
      • Cella D.F.
      • Perry S.W.
      Reliability and concurrent validity of three visual-analogue mood scales.
      The post diary also asked participants to indicate how many minutes were spent in completing the day's yoga practice assignment.
      An important requirement for the effective use of diary measures is that participants receive adequate training in the completion of diaries.
      • Bolger N.
      • Davis A.
      • Rafaeli E.
      Diary methods: capturing life as it is lived.
      Participants in this study were trained in how to complete the diary by a research assistant who helped them complete sample diaries. Patients also were called during the first week of each recording period to inquire about any difficulties and to answer any questions. Another key requirement of most daily-diary studies is that each day's responses be recorded by the end of that day.
      • Affleck G.
      • Urrows S.
      • Tennen H.
      • Higgins P.
      Daily coping with pain from rheumatoid arthritis: patterns and correlates.
      To bolster this expectation, we asked participants to mail each day's diary back to us the following morning in preaddressed stamped envelopes. To further facilitate motivation and compliance, patients were paid $0.25 for each completed daily diary and a $1.50 bonus for each week of complete recording. The diary completion rate was 89% (324 of 364 potentially reportable days across 13 participants; range, 71–100%). On average, patients completed 12 of the 14 diaries at both pre and post (SD=2).

      Focus Group Feedback

      After all participants had completed the intervention, the women were invited to a focus group meeting to give qualitative feedback regarding the Yoga of Awareness Program. Ten of the 13 participants attended. Open-ended questions were used to explore women's experiences regarding the various yoga methods used, the length and number of sessions, and the overall program. Women were invited to offer suggestions for how the program could be better tailored to their needs.

      Focus Group Anonymous Questionnaire

      Focus group participants were also asked to rate the success of the program on a five-item anonymous questionnaire. The questionnaire asked patients to rate, on 10-point Likert-type scales, how helpful the program was overall, how successful the program was in helping cope with feelings of distress, how successful the program was in helping manage pain, how successful the program was in helping manage fatigue, and whether they would recommend the program to a friend who has similar concerns.

      Yoga of Awareness Program

      The intervention consisted of eight weekly group sessions (four to five patients per group) conducted at the Duke Pain Prevention and Treatment Research Program offices. The groups were jointly led by a certified yoga teacher (registered with the national Yoga Alliance) who holds a master's degree in health behavior and education (KMC) and a clinical health psychologist (JWC). Both intervention leaders had received comprehensive training in traditional schools of yoga and had extensive experience in teaching yoga and meditation techniques to medical patients and the general public. On average, participants attended seven of the eight sessions (range, five to eight). To ensure consistency in delivering the intervention, a manual was developed to delineate the program and provide detailed session guidelines to be followed by the intervention leaders. All sessions were videotaped and reviewed in weekly treatment team meetings.
      Yoga of Awareness is an innovative behavioral intervention specifically designed and tailored to address patients' pain, fatigue, and emotional distress. The intervention is based in the ancient Indian discipline of yoga (meaning “yoking” or “union”). During recent years, as the physical exercises of yoga have become popularized in Western countries, the term yoga in common usage has largely become synonymous with this single aspect of the fuller discipline. Yoga in actuality comprises a wide variety of methods and approaches.
      • Cohen L.
      • Warneke C.
      • Fouladi R.T.
      • Rodriguez M.A.
      • Chaoul-Reich A.
      Psychological adjustment and sleep quality in a randomized controlled trial of the effects of a Tibetan yoga intervention in patients with lymphoma.
      • Feuerstein G.
      The yoga tradition: Its history, literature, philosophy and practice.
      The Yoga of Awareness intervention is a comprehensive yoga program that systematically integrates a broad spectrum of traditional yogic techniques and tenets. Each 120-minute session included gentle physical stretching postures (asanas, e.g., seated forward folds, supine lateral twists) complemented by breathing exercises (pranayama, e.g., extended exhalation, breathing into sensation), meditation techniques (dhyana, e.g., awareness of breath, awareness of awareness itself), study of pertinent topics (swadhyaya, e.g., themes such as the value of watching oneself in one's daily life with the intention to understand rather than to judge and of maintaining one's poise even amid the tumult of ever-changing challenges), and group discussions (satsang, e.g., discussion of experiences of practicing yoga at home, changes in cancer-related symptoms during the week). Patients were supplied with a yoga mat, a blanket, CDs/audiotapes, and illustrated handbooks to guide them in home practice. Participants were encouraged to spend at least 10 minutes a day practicing yoga strategies on their own, and applications of yoga to daily living were assigned each week (e.g., acceptance during intervals of pain).
      During sessions, the intervention leaders emphasized the importance of gentle posture practice when one's body is challenged by chronic illness, and instructions were modified to appropriately address individual patient needs (e.g., backache). Although the yoga postures used in this study presented no more risk of permanent injury than is associated with everyday activities such as climbing stairs or kneeling down to pick something up, nonetheless, as a precaution, a physician assistant or nurse was present during all sessions to address any medical concerns that may have arisen. However, their medical services were never needed. [Please contact the first author for a full description of the yoga postures used in the study.]

      Results

      Because of the preliminary nature of this study, analyses of outcome measures were based on data from study completers only.
      • Carson J.W.
      • Keefe F.J.
      • Lynch T.R.
      • et al.
      Loving-kindness meditation for chronic low back pain: results from a pilot trial.
      • Carson J.W.
      • Carson K.M.
      • Gil K.M.
      • Baucom D.H.
      Mindfulness-based relationship enhancement.
      A series of regression and Chi-square analyses comparing study completers and those who withdrew (either prior to or soon after beginning the intervention) indicated no significant differences in demographic characteristics. However, a significant effect was found for mean baseline scores on fatigue (F[1, 19]=8.26, P<0.01). Those who withdrew were likely to have lower scores on fatigue (M=46.92 for completers vs. 26.15 for noncompleters). There were also findings approaching significance for noncompleters to have higher baseline scores on relaxation (M=45.21 for completers vs. 63.16 for noncompleters, F[1, 19]=3.89, P=0.06) and invigoration (M=39.99 for completers vs. 54.58 for noncompleters, F[1, 19]=3.19, P=0.09) and lower scores on pain (M=33.92 for completers vs. 21.53 for noncompleters, F[1, 19]=2.65, P=0.12). Note that statistical power for these tests was low due to the small sample size.

      Approach to Multilevel Data Analyses

      The analyses for this study are based on a set of recently developed statistical procedures called multilevel modeling.
      • Kreft I.
      • de Leeuw J.
      Introducing multilevel modeling.
      Multilevel modeling is an advanced methodology for integrating data from multiple levels of sampling, such as this study's two levels (within-person and between-persons). Multilevel models are particularly advantageous in analyzing data sets with many repeated measures, such as daily-diary records.
      • Schwartz J.E.
      • Stone A.A.
      Strategies for analyzing ecological momentary assessment data.
      • Carson J.W.
      • Carson K.M.
      • Gil K.M.
      • Baucom D.H.
      Mindfulness-based relationship enhancement.
      By preserving the rich detail in each individual's full data set, multilevel models allow for a sensitive independent determination of day-to-day interrelated happenings for each patient, as well as aggregation of individual estimates for reliable results for the average patient. The SAS Proc Mixed procedure
      • SAS Institute
      SAS/STAT software: Changes and enhancements through release 6.12.
      produced parameters in the form of unstandardized maximum likelihood estimates (β coefficients). These are partial correlations, adjusted for between-person differences, which serve as effect size estimates of magnitude and direction of changes in dependent variables associated with changes in independent variables.
      • Bryk A.S.
      • Raudenbush S.W.
      Application of hierarchical linear models to assessing change.
      Multilevel models allow for strict control for potential confounds, such as serial autocorrelation in measurements. For all analyses, we allowed intercepts to vary randomly, thus allowing us to generalize the findings to the population of persons from which the sample was taken and the population of observations from which their daily reports were drawn.
      • Affleck G.
      • Zautra A.
      • Tennen H.
      • Armeli S.
      Multilevel daily process designs for consulting and clinical psychology: a preface for the perplexed.
      [For a more complete description of the multilevel equations reported herein, please contact the first author.]

      Treatment Effects on Daily Outcomes

      To examine treatment effects, models tested whether patients' intercept levels for daily pain, fatigue, distress, invigoration, acceptance, and relaxation changed significantly across time from the pre to the post recording periods.
      • Affleck G.
      • Zautra A.
      • Tennen H.
      • Armeli S.
      Multilevel daily process designs for consulting and clinical psychology: a preface for the perplexed.
      • Carson J.W.
      • Carson K.M.
      • Gil K.M.
      • Baucom D.H.
      Mindfulness-based relationship enhancement.
      Table 1 shows the outcomes for the effect of treatment (Time). Despite the small sample size, the results demonstrated significant improvements in daily invigoration and acceptance, along with trends for improvement in pain and relaxation.
      Table 1Multilevel Random Effects Estimates for Baseline Intercept and Effect of Treatment (Time)
      PredictorβtP
      Daily pain
       Baseline intercept34.628.38<0.01
      P≤0.01.
       Treatment (time)−3.26−1.720.10
      P≤0.10.
      Daily fatigue
       Baseline intercept46.7711.81<0.01
      P≤0.01.
       Treatment (time)−3.29−1.450.16
      Daily distress
       Baseline intercept35.4910.09<0.01
      P≤0.01.
       Treatment (time)1.660.780.44
      Daily invigoration
       Baseline intercept39.4612.46<0.01
      P≤0.01.
       Treatment (time)6.963.44<0.01
      P≤0.01.
      Daily acceptance
       Baseline intercept58.7311.71<0.01
      P≤0.01.
       Treatment (time)4.272.69<0.02
      P≤0.05.
      Daily relaxation
       Baseline intercept44.1513.20<0.01
      P≤0.01.
       Treatment (time)3.741.740.09
      P≤0.10.
      a P0.01.
      b P0.10.
      c P0.05.

      Length of Yoga Practice and Same Day Outcomes

      On 71% (SD=25%) of post diaries (collected during the last 14 days of the intervention), patients reported spending some time formally practicing yoga techniques. On average, they reported practicing for 21 minutes per day (SD=11). Analyses examined whether the number of minutes spent in yoga practice were predictive of same-day levels of diary variables. These models controlled for individuals' mean levels of yoga practice, and practice rates were person-centered to control for potentially spurious within-person associations.
      • Bryk A.S.
      • Raudenbush S.W.
      Application of hierarchical linear models to assessing change.
      Table 2 presents the results of these tests. Same-day tests indicated greater yoga practice was significantly associated with decreased pain, increased invigoration, and increased acceptance. Trends were also present for greater yoga practice to be associated with decreased fatigue (P=0.07) and increased relaxation (P=0.07).
      Table 2Multilevel Random Effects Estimates for Associations of Length of Yoga Practice with Day-to-Day Outcomes
      VariableSame Day OutcomesNext Day Outcomes
      βtPβtP
      Daily pain−0.15−2.71<0.01
      P≤0.01.
      −0.13−2.190.03
      P≤0.05.
      Daily fatigue−0.11−1.810.07
      P≤0.10.
      −0.13−1.960.05
      P≤0.05.
      Daily distress−0.04−0.600.550.010.040.97
      Daily invigoration0.162.99<0.01
      P≤0.01.
      0.213.41<0.01
      P≤0.01.
      Daily acceptance0.112.54<0.02
      P≤0.05.
      0.112.340.02
      P≤0.05.
      Daily relaxation0.111.830.07
      P≤0.10.
      0.142.180.03
      P≤0.05.
      a P0.01.
      b P0.05.
      c P0.10.

      Length of Yoga Practice and Lagged Day Outcomes

      The preceding same-day analyses did not address the question of temporal precedence and hence cannot be used to make causal inferences. Yoga practice potentially could have influenced levels of pain, invigoration, and acceptance, or the reverse could be true. Therefore, to clarify whether increases in yoga practice preceded and may have had a causative influence on day-to-day fluctuations in outcome variables, tests were conducted for lags of one and two days' practice. In lagged models, along with controlling for individuals' mean levels of practice, the lagged day's level of the dependent variable was also included as a within-person control variable (e.g., the present day's pain when predicting next day's pain). As before, practice rates were person-centered to control for any spurious within-person associations.
      The results for next-day lagged associations are shown in Table 2. Increased yoga practice was significantly predictive of improved levels of next-day pain, fatigue, invigoration, acceptance, and relaxation. For invigoration and acceptance, there were also trends for improved levels on the second day (not shown in Table 2; for invigoration, b=0.11, t=1.82, P=0.07; for acceptance, b=0.08, t=1.64, P=0.10).

      Focus Group Feedback

      Patients' responses to open-ended questions during the focus group meeting revealed a widespread consensus that the number and length of the yoga sessions, the techniques imparted, and the overall content of the program were appropriate and very useful. Comments included “The yoga program got me through a bad time and I am still applying the life skills I learned. I'm finding how to keep my balance even when the waves get rough,” and “The program really helped me become more aware of my body and to adjust to the changes that were happening. I learned to be more kind to myself.” Yet another woman said, “This program was extremely helpful. It made me realize how uptight I had become and how to deal with it. It also helped me deal with pain.” Women also remarked on the value of going through the yoga training in the company of other women who were contending with the unique challenges of MBC, as opposed to a more heterogeneous group: “It was great to be part of a group [that] has the same problems and concerns and we could truly understand one another's feelings.” Regarding suggestions for how the yoga training could be improved, several women indicated that it would be helpful if the program could be extended to include ongoing monthly yoga classes, as this would allow them to continue to build on their yoga practice and to share this experience with other women with MBC.

      Means of Focus Group Anonymous Questionnaire

      The means for the five items, all rated on 10-point scales, of the focus group anonymous questionnaire were as follows: how helpful the program was overall, M=9.6 (range, 8–10); how successful the program was in helping cope with feelings of distress, M=9 (range, 7–10); how successful the program was in helping manage pain, M=8 (range, 6–10); how successful the program was in helping manage fatigue, M=7.6 (range, 6–9); and whether they would recommend the program to a friend who has similar concerns M=10 (all scores were 10). Thus, patients' scores indicated that they generally perceived the program as very helpful in addressing the concerns targeted by the intervention.

      Discussion

      This pilot study examined the impact of a novel, yoga-based palliative intervention in a sample of MBC patients. Our findings, though very preliminary, suggest the intervention was helpful in significantly boosting daily invigoration and a sense of acceptance in patients. There were also trends for improvements in pain and relaxation. Moreover, a dose/response relationship was observed between day-to-day variations in patients' length of yoga practice and their daily symptoms and processes. Patients who practiced yoga longer on a given day were much more likely to experience lower pain and greater invigoration and acceptance that same day. Furthermore, patients who practiced longer on a given day were also much more likely to experience lower pain and fatigue and greater invigoration, acceptance, and relaxation on the next day. Although yoga has been used for centuries to treat disease in the East,
      • Telles S.
      • Naveen K.V.
      Yoga for rehabilitation: an overview.
      only recently have researchers begun to demonstrate yoga's effects on patients with cancer
      • Cohen L.
      • Warneke C.
      • Fouladi R.T.
      • Rodriguez M.A.
      • Chaoul-Reich A.
      Psychological adjustment and sleep quality in a randomized controlled trial of the effects of a Tibetan yoga intervention in patients with lymphoma.
      • Culos-Reed S.N.
      • Carlson L.E.
      • Daroux L.M.
      • Hately-Aldous S.
      A pilot study of yoga for breast cancer survivors: physical and psychological benefits.
      • Joseph C.D.
      Psychological supportive therapy for cancer patients.
      and various other conditions (e.g., osteoarthritis, low back pain, multiple sclerosis
      • Garfinkel M.S.
      • Schumacher Jr., H.R.
      • Husain A.
      • Levy M.
      • Reshetar R.A.
      Evaluation of a yoga based regimen for treatment of osteoarthritis of the hands.
      • Oken B.S.
      • Kishiyama S.
      • Zajdel D.
      • et al.
      Randomized controlled trial of yoga and exercise in multiple sclerosis.
      • Williams K.A.
      • Petronis J.
      • Smith D.
      • et al.
      Effect of Iyengar yoga therapy for chronic low back pain.
      ). Heretofore, no studies have reported on yoga's effects in MBC patients. This study provides some of the first, tentative evidence for yoga's potential benefits in this vulnerable population of women with limited life expectancy.
      Because of the absence of a control group, it is difficult to directly compare the magnitude of our findings with those of other palliative intervention studies in MBC patients. As noted above, however, significant findings with this population have often consisted of less increase in symptoms in the intervention vs. control conditions rather than actual improvements.
      • Bordeleau L.
      • Szalai J.P.
      • Ennis M.
      • et al.
      Quality of life in a randomized trial of group psychosocial support in metastatic breast cancer: overall effects of the intervention and an exploration of missing data.
      • Goodwin P.J.
      • Leszcz M.
      • Ennis M.
      • et al.
      The effect of group psychosocial support on survival in metastatic breast cancer.
      • Spiegel D.
      • Bloom J.R.
      Group therapy and hypnosis reduce metastatic breast carcinoma pain.
      • Spiegel D.
      • Bloom J.R.
      • Kraemer H.C.
      • Gottheil E.
      Effect of psychosocial treatment on survival of patients with metastatic breast cancer.
      • Headley J.A.
      • Ownby K.K.
      • John L.D.
      The effect of seated exercise on fatigue and quality of life in women with advanced breast cancer.
      So, while the absence of a control group does not allow us to test for differential decline in symptoms, the fact that the treatment-related coefficients for daily pain, fatigue, invigoration, acceptance, and relaxation (with the sole exception of daily distress) were in the direction of true improvements has important implications for the potential efficacy of the intervention.
      Beyond examining the effects of the yoga-based intervention, this study marks the first time multilevel modeling has been applied to daily-diary outcomes in MBC patients. Importantly, the present multilevel treatment results were obtained by first calculating independent estimates for each participant and then aggregating them to derive reliable results for the average patient—thus avoiding the problem of overlooking the impact of individual differences, as in standard regression approaches. Moreover, the advantages offered by this statistical approach were particularly well suited for the analysis of real-time processes that have strong causal implications. The tangible impact of yoga practice was highlighted by the finding that greater practice on a given day was associated with improvements not only on the same day, but the next day as well. Future studies could profit from using daily data collection to examine more refined hypotheses about changes in patients' symptoms (e.g., would yoga lead to same-day or next-day fatigue becoming more resilient to the negative impact of a chemotherapy session
      • Irvine D.
      • Vincent L.
      • Graydon J.E.
      • Bubela N.
      • Thompson L.
      The prevalence and correlates of fatigue in patients receiving treatment with chemotherapy and radiotherapy.
      ).
      Attrition in this study was similar to previous palliative trials for MBC.
      • Edelman S.
      • Bell D.R.
      • Kidman A.D.
      A group cognitive behaviour therapy programme with metastatic breast cancer patients.
      • Goodwin P.J.
      • Leszcz M.
      • Ennis M.
      • et al.
      The effect of group psychosocial support on survival in metastatic breast cancer.
      • Spiegel D.
      • Bloom J.R.
      Group therapy and hypnosis reduce metastatic breast carcinoma pain.
      • Headley J.A.
      • Ownby K.K.
      • John L.D.
      The effect of seated exercise on fatigue and quality of life in women with advanced breast cancer.
      Analyses showed that completers tended to be patients who were experiencing higher levels of fatigue and other outcomes—presumably because these women were more highly motivated by the possibility of ameliorating their symptoms. In contrast, in the only previous psychosocial intervention study to report on a comparison of completers and noncompleters, a trial of cognitive-behavioral group therapy, Edelman et al. found the opposite: the noncompleters tended to be patients with greater symptom levels (e.g., higher anxiety, lower vigor).
      • Edelman S.
      • Bell D.R.
      • Kidman A.D.
      A group cognitive behaviour therapy programme with metastatic breast cancer patients.
      The Yoga of Awareness intervention we used, which comprehensively integrates a wide spectrum of ancient yoga techniques—postures, breathing exercises, meditation, study of guiding tenets, and group discussions—stands in strong contrast to previous palliative interventions with MBC patients, such as cognitive-behavioral group therapy and supportive-expressive group therapy.
      • Cunningham A.J.
      • Edmonds C.V.
      • Jenkins G.P.
      • et al.
      A randomized controlled trial of the effects of group psychological therapy on survival in women with metastatic breast cancer.
      • Edelman S.
      • Bell D.R.
      • Kidman A.D.
      A group cognitive behaviour therapy programme with metastatic breast cancer patients.
      • Edelman S.
      • Lemon J.
      • Bell D.R.
      • Kidman A.D.
      Effects of group CBT on the survival time of patients with metastatic breast cancer.
      • Edmonds C.V.
      • Lockwood G.A.
      • Cunningham A.J.
      Psychological response to long-term group therapy: a randomized trial with metastatic breast cancer patients.
      • Bordeleau L.
      • Szalai J.P.
      • Ennis M.
      • et al.
      Quality of life in a randomized trial of group psychosocial support in metastatic breast cancer: overall effects of the intervention and an exploration of missing data.
      • Classen C.
      • Butler L.D.
      • Koopman C.
      • et al.
      Supportive-expressive group therapy and distress in patients with metastatic breast cancer: a randomized clinical intervention trial.
      • Goodwin P.J.
      • Leszcz M.
      • Ennis M.
      • et al.
      The effect of group psychosocial support on survival in metastatic breast cancer.
      • Spiegel D.
      • Bloom J.R.
      • Yalom I.
      Group support for patients with metastatic cancer.
      • Spiegel D.
      • Bloom J.R.
      Group therapy and hypnosis reduce metastatic breast carcinoma pain.
      • Spiegel D.
      • Bloom J.R.
      • Kraemer H.C.
      • Gottheil E.
      Effect of psychosocial treatment on survival of patients with metastatic breast cancer.
      This intervention also contrasts with some yoga trainings that have been used with cancer patients, which emphasize only one component of the yoga system, that is, the posture exercises that have become widely popularized in Western countries (e.g., Culos-Reed et al.
      • Culos-Reed S.N.
      • Carlson L.E.
      • Daroux L.M.
      • Hately-Aldous S.
      A pilot study of yoga for breast cancer survivors: physical and psychological benefits.
      ). Notably, however, only a minority of the participants in our study had ever practiced yoga or meditation before, and among this minority, only a few had more than minimal exposure to these methods. Despite this unfamiliarity, our findings clearly demonstrated the feasibility of conducting future studies of the Yoga of Awareness Program with MBC patients. It is important to note that four of the 13 women in our sample experienced new cancer recurrences during the study, and the physical condition of several others was noticeably deteriorating. Nonetheless, no adverse events were related to yoga participation. It is likely that the gentle approach to yoga postures we used, including careful monitoring of teaching methods in weekly treatment team meetings, was vital to making the yoga program safe for these women. In addition, attendance at yoga sessions during the study was good (an average of seven of eight sessions), as was adherence to yoga practice (an average of 21 minutes per day). Further confirmation of the feasibility of offering this program to MBC patients came from the focus group meeting. Along with giving the program high ratings on the anonymous questionnaire, participants' comments confirmed the suitability of the yoga intervention's content and the number and length of yoga sessions. The only drawback patients noted was that the program did not lead to an ongoing opportunity to practice yoga in the company of other women with MBC. Future studies should consider ways to create a structure for continuing specialized yoga classes past the study termination. Finally, patients' anecdotal reports revealed that the yoga training appeared to be very useful in helping them better adjust to the challenges of living with metastatic disease, including “keeping their balance even when the waves get rough.”
      Several important limitations of our study should be noted. The generalizability of these preliminary findings is restricted by the very small sample, the absence of a control group, and the lack of follow-up data. To clearly establish the efficacy of the Yoga of Awareness Program, a controlled (e.g., support group control), well-powered trial including follow-up evaluations is needed. Further methodological improvements for such a study could include supplementation of self-report data by other types of measures (e.g., immune response,
      • Giese-Davis J.
      • Sephton S.E.
      • Abercrombie H.C.
      • Duran R.E.
      • Spiegel D.
      Repression and high anxiety are associated with aberrant diurnal cortisol rhythms in women with metastatic breast cancer.
      • van der Pompe G.
      • Antoni M.
      • Visser A.
      • Garssen B.
      Adjustment to breast cancer: the psychobiological effects of psychosocial interventions.
      physical fitness
      • Culos-Reed S.N.
      • Carlson L.E.
      • Daroux L.M.
      • Hately-Aldous S.
      A pilot study of yoga for breast cancer survivors: physical and psychological benefits.
      ), formal analyses of treatment integrity,
      • Waltz J.
      • Addis M.E.
      • Koerner K.
      • Jacobson N.S.
      Testing the integrity of a psychotherapy protocol: assessment of adherence and competence.
      and analyses of predictors of treatment outcome (e.g., is yoga more helpful for patients with certain characteristics). Future studies can also seek to determine minimum amounts of effective yoga practice, and given the dose/response effect observed, how adherence can be bolstered in those who practice less.
      In conclusion, the findings of this pilot study provide promising preliminary support for the palliative health benefits of yoga in MBC patients. The improvements that have been documented, and the potential impact these improvements may have on patients' adjustment during the remaining years of their lives, are important enough to warrant further study.

      References

        • Leonard R.C.
        • Rodger A.
        • Dixon J.M.
        • Dixon J.M.
        Metastatic breast cancer.
        in: Dixon M. ABC of breast diseases. 2nd ed. BMJ Books, London2000: 65-71
        • Aranda S.
        • Schofield P.
        • Weih L.
        • et al.
        Mapping the quality of life and unmet needs of urban women with metastatic breast cancer.
        Eur J Cancer Care. 2005; 14: 211-222
        • Cella D.
        Factors influencing quality of life in cancer patients: anemia and fatigue.
        Semin Oncol. 1998; 25: 43-46
        • Patrick D.L.
        • Ferketich S.L.
        • Frame P.S.
        • et al.
        National Institutes of Health State-of-the-science conference statement: symptom management in cancer: pain, depression, and fatigue.
        J Natl Cancer Inst. 2003; 95: 1110-1117
        • Rowland J.H.
        • Massie M.J.
        • Holland J.C.
        Breast cancer.
        in: Holland J.C. Breitbart W. Jacobsen P.B. Lederberg M.S. Psycho-oncology. Oxford University Press, New York1998: 380-401
        • Foley K.M.
        • Arbit E.
        • DeVita V.T.
        • Hellman S.
        • Rosenberg S.A.
        Management of cancer pain.
        in: DeVita V.T. Rosenberg S.A. Hellman S. Principles and practice of oncology. 3rd ed. J.B. Lippincott, Philadelphia1989: 2064-2087
        • Osoba D.
        • Slamon D.J.
        • Burchmore M.
        • et al.
        Effects on quality of life of combined trastuzumab and chemotherapy in women with metastatic breast cancer.
        J Clin Oncol. 2002; 20: 3106-3113
        • Cunningham A.J.
        • Edmonds C.V.
        • Jenkins G.P.
        • et al.
        A randomized controlled trial of the effects of group psychological therapy on survival in women with metastatic breast cancer.
        Psychooncology. 1998; 7: 508-517
        • Edelman S.
        • Bell D.R.
        • Kidman A.D.
        A group cognitive behaviour therapy programme with metastatic breast cancer patients.
        Psychooncology. 1999; 8: 295-305
        • Edelman S.
        • Lemon J.
        • Bell D.R.
        • Kidman A.D.
        Effects of group CBT on the survival time of patients with metastatic breast cancer.
        Psychooncology. 1999; 8: 474-481
        • Edmonds C.V.
        • Lockwood G.A.
        • Cunningham A.J.
        Psychological response to long-term group therapy: a randomized trial with metastatic breast cancer patients.
        Psychooncology. 1999; 8: 74-91
        • Bordeleau L.
        • Szalai J.P.
        • Ennis M.
        • et al.
        Quality of life in a randomized trial of group psychosocial support in metastatic breast cancer: overall effects of the intervention and an exploration of missing data.
        J Clin Oncol. 2003; 21: 1944-1951
        • Classen C.
        • Butler L.D.
        • Koopman C.
        • et al.
        Supportive-expressive group therapy and distress in patients with metastatic breast cancer: a randomized clinical intervention trial.
        Arch Gen Psychiatry. 2001; 58: 494-501
        • Goodwin P.J.
        • Leszcz M.
        • Ennis M.
        • et al.
        The effect of group psychosocial support on survival in metastatic breast cancer.
        N Engl J Med. 2001; 345: 1719-1726
        • Spiegel D.
        • Bloom J.R.
        • Yalom I.
        Group support for patients with metastatic cancer.
        Arch Gen Psychiatry. 1981; 38: 527-533
        • Spiegel D.
        • Bloom J.R.
        Group therapy and hypnosis reduce metastatic breast carcinoma pain.
        Psychosom Med. 1983; 45: 333-339
        • Spiegel D.
        • Bloom J.R.
        • Kraemer H.C.
        • Gottheil E.
        Effect of psychosocial treatment on survival of patients with metastatic breast cancer.
        Lancet. 1989; 2: 888-891
        • Edwards A.G.
        • Hailey S.
        • Maxwell M.
        Psychological interventions for women with metastatic breast cancer.
        Cochrane Database Syst Rev. 2004; (CD004253)
        • Headley J.A.
        • Ownby K.K.
        • John L.D.
        The effect of seated exercise on fatigue and quality of life in women with advanced breast cancer.
        Oncol Nurs Forum. 2004; 31: 977-983
        • Telles S.
        • Naveen K.V.
        Yoga for rehabilitation: an overview.
        Indian J Med Sci. 1997; 51: 123-127
      1. Alferi SM, Antoni MH, Ironson G, Kilbourn KM, Carver CS. Factors predicting the use of complementary therapies in a multi-ethnic sample of early-stage breast cancer patients. J Am Med Womens Assoc. 2001;56:120–123.

        • Eisenberg D.M.
        • Davis R.B.
        • Ettner S.L.
        • et al.
        Trends in alternative medicine use in the United States, 1990–1997: results of a follow-up national survey.
        JAMA. 1998; 280: 1569-1575
        • Lee M.M.
        • Lin S.S.
        • Wrensch M.R.
        • Adler S.R.
        • Eisenberg D.
        Alternative therapies used by women with breast cancer in four ethnic populations.
        J Natl Cancer Inst. 2000; 92: 42-47
        • Richardson M.A.
        • Sanders T.
        • Palmer J.L.
        • Greisinger A.
        • Singletary S.E.
        Complementary/alternative medicine use in a comprehensive cancer center and the implications for oncology.
        J Clin Oncol. 2000; 18 ([see comment]): 2505-2514
        • Bower J.E.
        • Woolery A.
        • Sternlieb B.
        • Garet D.
        Yoga for cancer patients and survivors.
        Cancer Control. 2005; 12: 165-171
        • Brawley L.R.
        • Culos-Reed S.N.
        • Angove J.
        • Hoffman-Goetz L.
        Understanding the barriers to physical activity for cancer patients: review and recommendations.
        J Psychosoc Oncol. 2002; 20: 1-21
        • Cohen L.
        • Warneke C.
        • Fouladi R.T.
        • Rodriguez M.A.
        • Chaoul-Reich A.
        Psychological adjustment and sleep quality in a randomized controlled trial of the effects of a Tibetan yoga intervention in patients with lymphoma.
        Cancer. 2004; 100: 2253-2260
        • Culos-Reed S.N.
        • Carlson L.E.
        • Daroux L.M.
        • Hately-Aldous S.
        A pilot study of yoga for breast cancer survivors: physical and psychological benefits.
        Psycho-Oncol. 2006; 15: 891-897
        • Joseph C.D.
        Psychological supportive therapy for cancer patients.
        Indian J Cancer. 1983; 20: 268-270
        • Wood C.
        Mood change and perceptions of vitality: a comparison of the effects of relaxation, visualization and yoga.
        J R Soc Med. 1993; 86: 254-258
        • McCracken L.M.
        • Carson J.W.
        • Eccleston C.
        • Keefe F.J.
        Acceptance and change in the context of chronic pain.
        Pain. 2004; 109: 4-7
        • Clark D.
        Between hope and acceptance: the medicalisation of dying.
        BMJ. 2002; 324: 905-907
        • Kamei T.
        • Toriumi Y.
        • Kimura H.
        • et al.
        Decrease in serum cortisol during yoga exercise is correlated with alpha wave activation.
        Percept Mot Skills. 2000; 90: 1027-1032
        • Patel C.
        • North W.R.
        Randomised controlled trial of yoga and bio-feedback in management of hypertension.
        Lancet. 1975; 2: 93-95
        • Raghuraj R.
        • Telles S.
        Effect of a yoga-based and forced uninostril breathing on the autonomic nervous system.
        Percept Mot Skills. 2003; 96: 79-80
        • Schell F.J.
        • Allolio B.
        • Schonecke O.W.
        Physiological and psychological effects of Hatha-Yoga exercise in healthy women.
        Int J Psychosom. 1994; 41: 46-52
        • Telles S.
        • Reddy S.K.
        • Nagendra H.R.
        Oxygen consumption and respiration following two yoga relaxation techniques.
        Appl Psychophysiol Biofeedback. 2000; 25: 221-227
        • Telles S.
        • Joshi M.
        • Dash M.
        • et al.
        An evaluation of the ability to voluntarily reduce the heart rate after a month of yoga practice.
        Integr Physiol Behav Sci. 2004; 39: 119-125
        • Lehrer P.M.
        • Woolfolk R.L.
        Principles and practice of stress management.
        2nd ed. Guilford Press, New York1993
        • Nespor K.
        Pain management and yoga.
        Int J Psychosom. 1991; 38: 76-81
        • Carson J.W.
        • Keefe F.J.
        • Lynch T.R.
        • et al.
        Loving-kindness meditation for chronic low back pain: results from a pilot trial.
        J Holist Nurs. 2005; 23: 1-18
      2. Carson JW, Keefe FJ, Affleck G, et al. A comparison of conventional pain coping skills training and pain coping skills training with a maintenance training component: a daily diary analysis of short- and long-term treatment effects. J Pain 2006;7:615–625.

        • Stone A.A.
        • Kessler R.C.
        • Haythornthwaite J.A.
        Measuring daily events and experiences: decisions for the researcher.
        J Pers. 1991; 59: 575-607
        • Verbrugge L.M.
        Health diaries.
        Med Care. 1980; 18: 73-95
        • Bolger N.
        • Davis A.
        • Rafaeli E.
        Diary methods: capturing life as it is lived.
        Annu Rev Psychol. 2003; 54: 579-616
        • Affleck G.
        • Zautra A.
        • Tennen H.
        • Armeli S.
        Multilevel daily process designs for consulting and clinical psychology: a preface for the perplexed.
        J Consult Clin Psychol. 1999; 67: 746-754
        • Jaccard J.
        • Wan C.K.
        Statistical analysis of temporal data with many observations: issues for behavioral medicine data.
        Ann Behav Med. 1993; 15: 41-50
        • Schwartz J.E.
        • Stone A.A.
        Strategies for analyzing ecological momentary assessment data.
        Health Psychol. 1998; 17: 6-16
        • West S.G.
        • Hepworth J.T.
        Statistical issues in the study of temporal data: daily experiences.
        J Pers. 1991; 59: 609-662
        • Cella D.F.
        • Perry S.W.
        Reliability and concurrent validity of three visual-analogue mood scales.
        Psychol Rep. 1986; 59: 827-833
        • Affleck G.
        • Urrows S.
        • Tennen H.
        • Higgins P.
        Daily coping with pain from rheumatoid arthritis: patterns and correlates.
        Pain. 1992; 51: 221-229
        • Feuerstein G.
        The yoga tradition: Its history, literature, philosophy and practice.
        Shambala, Boston2001
        • Carson J.W.
        • Carson K.M.
        • Gil K.M.
        • Baucom D.H.
        Mindfulness-based relationship enhancement.
        Behav Ther. 2004; 35: 471-494
        • Kreft I.
        • de Leeuw J.
        Introducing multilevel modeling.
        Sage, London1998
        • SAS Institute
        SAS/STAT software: Changes and enhancements through release 6.12.
        SAS Institute, Cary, NC1996
        • Bryk A.S.
        • Raudenbush S.W.
        Application of hierarchical linear models to assessing change.
        Psychol Bull. 1987; 101: 147-158
        • Garfinkel M.S.
        • Schumacher Jr., H.R.
        • Husain A.
        • Levy M.
        • Reshetar R.A.
        Evaluation of a yoga based regimen for treatment of osteoarthritis of the hands.
        J Rheumatol. 1994; 21: 2341-2343
        • Oken B.S.
        • Kishiyama S.
        • Zajdel D.
        • et al.
        Randomized controlled trial of yoga and exercise in multiple sclerosis.
        Neurology. 2004; 62: 2058-2064
        • Williams K.A.
        • Petronis J.
        • Smith D.
        • et al.
        Effect of Iyengar yoga therapy for chronic low back pain.
        Pain. 2005; 115: 107-117
        • Irvine D.
        • Vincent L.
        • Graydon J.E.
        • Bubela N.
        • Thompson L.
        The prevalence and correlates of fatigue in patients receiving treatment with chemotherapy and radiotherapy.
        Cancer Nurs. 1994; 17: 367-378
        • Giese-Davis J.
        • Sephton S.E.
        • Abercrombie H.C.
        • Duran R.E.
        • Spiegel D.
        Repression and high anxiety are associated with aberrant diurnal cortisol rhythms in women with metastatic breast cancer.
        Health Psychol. 2004; 23: 645-650
        • van der Pompe G.
        • Antoni M.
        • Visser A.
        • Garssen B.
        Adjustment to breast cancer: the psychobiological effects of psychosocial interventions.
        Patient Educ Couns. 1996; 28: 209-219
        • Waltz J.
        • Addis M.E.
        • Koerner K.
        • Jacobson N.S.
        Testing the integrity of a psychotherapy protocol: assessment of adherence and competence.
        J Consult Clin Psychol. 1993; 61: 620-630