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Yoga management of breast cancer-related lymphoedema: a randomised controlled pilot-trial

Yoga management of breast cancer-related lymphoedema: a randomised controlled pilot-trial Background: Secondary arm lymphoedema continues to affect at least 20% of women after treatment for breast cancer requiring lifelong professional treatment and self-management. The holistic practice of yoga may offer benefits as an adjunct self-management option. The aim of this small pilot trial was to gain preliminary data to determine the effect of yoga on women with stage one breast cancer-related lymphoedema (BCRL). This paper reports the results for the primary and secondary outcomes. Methods: Participants were randomised, after baseline testing, to receive either an 8-week yoga intervention (n = 15), consisting of a weekly 90-minute teacher-led class and a 40-minute daily session delivered by DVD, or to a usual care wait-listed control group (n = 13). Primary outcome measures were: arm volume of lymphoedema measured by circumference and extra-cellular fluid measured by bioimpedance spectroscopy. Secondary outcome measures were: tissue induration measured by tonometry; levels of sensations, pain, fatigue, and their limiting effects all measured by a visual analogue scale (VAS) and quality of life based on the Lymphoedema Quality of Life Tool (LYMQOL). Measurements were conducted at baseline, week 8 (post-intervention) and week 12 (four weeks after cessation of the intervention). Results: At week 8, the intervention group had a greater decrease in tissue induration of the affected upper arm compared to the control group (p = 0.050), as well as a greater reduction in the symptom sub-scale for QOL (p = 0.038). There was no difference in arm volume of lymphoedema or extra-cellular fluid between groups at week 8; however, at week 12, arm volume increased more for the intervention group than the control group (p = 0.032). Conclusions: An 8-week yoga intervention reduced tissue induration of the affected upper arm and decreased the QOL sub-scale of symptoms. Arm volume of lymphoedema and extra-cellular fluid did not increase. These benefits did not last on cessation of the intervention when arm volume of lymphoedema increased. Further research trials with a longer duration, higher levels of lymphoedema and larger numbers are warranted before definitive conclusions can be made. Keywords: Yoga, Breast cancer-related lymphoedema, Symptoms, Quality of life, Randomised controlled trial Background As well as fibrosis of the tissue and increased risk of Breast cancer is the second most common form of cancer infection [4], women with BCRL can experience a range in women after skin cancer, and its incidence is expected of debilitating sensations and symptoms [5,6] and in com- to rise due to the ageing population [1]. In spite of parison to women who have had breast cancer treatment improvements to surgical and radiotherapy treatment, without lymphoedema, have impaired physical function at least 20% of treated women will continue to be diagnosed [7] and lower quality of life (QOL) [8]. with breast cancer-related lymphoedema (BCRL) [2] that Due to the multi-dimensional consequences of BCRL, requires lifelong treatment and management [3]. a holistic management approach, including exercise, is recommended [3]. Previously, exercise participation was discouraged due to concerns that exercise may exacerbate the condition; however, there is growing evidence to * Correspondence: Andrew.Williams@utas.edu.au support the use of progressive and supervised exercise School of Health Sciences, University of Tasmania, Launceston, Australia Full list of author information is available at the end of the article © 2014 Loudon et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 2 of 13 http://www.biomedcentral.com/1472-6882/14/214 for women with BCRL with adequate warm-up, cool-down, and data collection sessions were held in Community appropriate rests [9] and suitable training of staff [10]. This Health Centres at two locations, Hobart and Launceston, evidence comes from studies covering a range of exercise between February and May 2011. Both locations consisted modalities, which have reported no increase in severity of an intervention and control group. [11,12] and fewer exacerbations of lymphoedema [13], Randomisation was conducted by a person not associated increased strength [13], reductions in symptoms [13,14], with the trial from a computer-generated random number and improvements in QOL [15,16]. In light of this, re- system (http://www.randomization.com). No stratification search into other holistic interventions, including yoga, occurred. Participants received notification of their group for women with BCRL has been recommended [6,9,14]. allocation in sealed envelopes after baseline testing. Yoga is a holistic system of practices that aims to create balance in the physical, mental and emotional self [17]. It Participants includes breathing (pranayama), postures (asana), medita- Eligibility criteria tion and relaxation. The physical movements and slow Women were eligible for inclusion if they had stage one breathing, which can be adapted to principles of lymphatic unilateral secondary lymphoedema of the arm, as defined clearing, have been used effectively as part of a holistic by the International Society of Lymphology [3] confirmed treatment to reduce lower limb lymphoedema from by a professional lymphoedema therapist, and had com- filariasis [18]. The practices of breathing, meditation pleted treatment for breast cancer (surgery, radiotherapy and relaxation have been reported to improve the psycho- and chemotherapy) at least six months previously, were social functioning of women during and after breast can- over 18 and had sufficient English literacy to provide in- cer treatment [19]. These outcomes may be transferrable formed consent. Briefly, stage one lymphoedema is de- to women with BCRL. Women with BCRL are already fined as early stage lymphoedema that will subside with attending yoga sessions [20], though the outcomes from elevation and may have signs of pitting and was chosen this have not been systematically investigated. for this trial for two principal reasons. Firstly, as this was The aim of this study was to obtain preliminary data the first 8-week pilot trial to use a yoga intervention, to determine the effect of yoga on women with BCRL. women’s safety was paramount and it was thought that This paper reports the results of the primary outcomes lower levels of lymphoedema may be more stable during of lymphoedema status and the secondary outcomes of the intervention period. Secondly, the standard offers a lymphoedema symptoms and QOL in women with stage definition that could be confirmed or negated by a quali- one BCRL. We hypothesised that yoga would reduce fied lymphoedema therapist to account for different swelling caused by lymphoedema relative to usual care methods of clinical measurement. Measurement of and would lead to a reduction in tissue induration and women to confirm lymphoedema status was not possible severity of sensations, pain and fatigue associated with lym- prior to baseline testing because non-metric measurement phoedema and their limiting effects, and improve QOL. equipment was not available to clinicians. Women were excluded if they had recurrent cancer, Methods an infection, were having Complex Lymphoedema Ther- Study design apy, if they were pregnant, wore a pacemaker, which The trial was a multi-centred randomised controlled pilot would affect bioimpedance spectroscopy (BIS) readings, trial using a parallel design with participants allocated to or had severe psychological illness. All participants in intervention or control on a 1:1 allocation ratio. The study the trial received a manual containing information on was registered with the Australian New Zealand Clinical best current care for BCRL. Women were advised not to Trials Registry and ethics approval was granted by the change current exercise nor commence any new activity University of Tasmania’s Social Sciences Human Research during the study period and to seek immediate medical Ethics Committee. This study was part of a larger mixed help if they experienced an exacerbation of lymphoe- methods study. The full protocol has been described pre- dema during the trial. viously [21]. This paper presents the results for the pri- mary outcomes of arm volume of lymphoedema and extra-cellular fluid and the secondary outcomes of tissue Control group induration, sensations and their limiting effects and QOL. Participants randomised to the control group maintained After meeting the selection criteria and giving informed their usual self-care as advised by their lymphoedema consent, participants were randomised to a yoga inter- therapist. Self-care included wearing of compression vention group or a wait-listed usual care control group. sleeves, self-massage, skin protection and continued Outcome measurements were performed at baseline usual lymphatic treatment. The control group were (week 0), week 8 (on completion of intervention) and at offered yoga classes at the completion of the final week 12 (one month after intervention). All intervention measurement. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 3 of 13 http://www.biomedcentral.com/1472-6882/14/214 Yoga intervention group fluid from BIS. These measures can give different outcomes Participants randomised to the intervention group attended [25,26]; for example, BIS results include the fluid in the a weekly 90-minute yoga class taught by an experienced upper part of the arm where it is difficult to get circumfer- and accredited yoga teacher with qualifications in yoga ential readings. therapy and Manual Lymphatic Drainage. Participants were Circumferential readings were taken by a Jobst non- also given a DVD with a 45-minute yoga session and stretch tape according to an established protocol [27] at the instructed to perform it daily. The DVD followed the same metacarpophalangeal joint and at 10 cm intervals from sequence of practices as the class, with fewer postures and the styloid process. Volume of arm lymphoedema was a shorter relaxation. Participants received a logbook in calculated using the truncated cone formula [28] from which they recorded their daily practice along with any the addition of circumferential readings using an Excel relevant comments. Women were given the choice to spreadsheet that compared the affected to the non-affected wear a compression sleeve and, if removed, instructed to arm, resulting in a measure of Absolute Arm Volume be- wear it again immediately after the yoga session [22]. tween the affected and non-affected arm. Measurements The yoga session included documented breathing were recorded in millilitres (ml). practices, physical postures, meditation and relaxation Extra-cellular fluid was measured by BIS L-dex XCA™ techniques according to the Satyananda Yoga® tradition (Bio-Impedimed, Queensland) [29]. Electrodes were placed [23] (Table 1). This style offers systematised practices at anatomical landmarks at the wrist of each arm and right and instruction thought to be suited to women with ankle to provide a low-frequency electrical current. An BCRL. Options for modifications were offered in the increase in extra-cellular fluid is paralleled by a decrease in class and DVD. The practices were chosen to promote impedance and the result recorded as a ratio to the non- lymphatic drainage and to reduce stress and conformed affected arm, taking into consideration arm dominance with exercise guidelines and precautions for women with [26]. The result was an L-dex reading, calculated from soft- BCRL [3,9]. A full rationale for the session and chosen ware provided by the manufacturer. practices has been provided previously [24]. Tissue induration Outcome measures Induration of fibrotic tissue was measured using a digital Measurements, based on validated instruments and pro- tonometer, model 1383 (Biomedical Engineering, Flinders tocols, were taken by trained researchers blinded to the Medical Centre, South Australia) [30]. The digital tonom- group allocation and previous results. Severity of lym- eter measures the resistance to compression in the superfi- phoedema for arm volume and extra-cellular fluid and cial tissues at a given point on the areas of lymph drainage tissue induration were measured by an experienced and (lymphatic territory) [25]. Measurements were taken 10 cm registered lymphoedema physiotherapist at each location. from the cubital fossa on the forearm and 10 cm from the Inter-rater reliability between lymphoedema therapists cubital fossa on the upper arm, in the middle of the areas was assessed pre-trial and rated as acceptable for variabil- of lymphatic territory. Anterior trunk measurements were ity’s between 2-3%. Other trained assessors administered taken at the mid-clavicular line between the second and anthropometric measurements and questionnaires at both third ribs and at the posterior trunk between the acromion places on different days. To ensure consistency at each and the first thoracic rib in the subscapular fossa. Measure- time-point, participants attended at the same time through- ments were taken three times at each position, separated by out the trial and the same assessor was responsible for each a three-second pause, for the affected and non-affected arm measure. Participants were requested to abstain from alco- and trunk. A higher score denoted a higher level of indur- hol for 12 hours and caffeine and exercise for two hours ation of fibrotic tissue. The average of three measurements before testing to increase the validity of the BIS readings. was recorded in millimetres (mm). On arrival at the testing facility, participants underwent anthropometric measurements wearing light clothes and Sensations, pain and fatigue and their limiting effects no footwear. Participants then underwent measures of Participants recorded the severity of sensations, pain and lymphoedema and tissue induration and completed VAS fatigue, and the degree to which sensations, pain and fa- and QOL questionnaires in the same order at each meas- tigue limited activity on the day of measurement on a urement session. 10 cm Visual Analogue Scale (VAS) [31]. A score of 0 cm indicated “no discomfort” and a score of 10 cm indicated Lymphoedema “the worst imaginable”. Lymphoedema was measured with the participant supine and arm dominance noted. Women removed their sleeve Quality of life on entering the measurement venue. Two measures were A validated questionnaire, developed specifically to meas- chosen: arm volume from circumference and extra-cellular ure QOL for people with arm lymphoedema, LYMQOL Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 4 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 1 Yoga session weeks 1–8 including on DVD Practice and time allocated Sanskrit Settling and Breathing 10 minutes (DVD 10 minutes) Settling with awareness Kaya Sthairyam [1] Mindfulness (inner silence) Antar Mouna level one [2] Abdominal, thoracic, clavicular breath Pranayama [3] Full yoga breath Pranayama [3] Postures 35 minutes (DVD 25 minutes) [3] 1a Neck turns Greeva Sanchalana 1b Add outward rotation of opposite arm Utthanpadasana-variation 3 Knee hugs-leg lock pose Supta Pawanmuktasana 4 Shoulder circles Shandha Chakra 5 Bent arm opening, chest towards knees Naukasana-variation combined with Namaskarasana-variation of arms 6 Lying Archer Akarna Dhanurasana-variation 7 Lying rotation Supta Udarakarshanasana-variation 8 Arm/leg stretch Supta Pawanmuktasana 9 Sitting rowing Nauka Sanchalanasana 10 Standing archer Akarna Dhanurasana 11 Modified rope climbing Rajju Karshanasana-variation 12 Modified arm raise, knee bend Tadasana-variation 13 Modified side bend Trikonasana-variation 14 Standing rotation Kati Chakrasana 15 Standing Cat Marjari-asana_variation 16 Modified one legged prayer balance Eka Pada Pranamasana 17 Sitting neck turns Greeva Sanchalana Mindfulness, Pranayama, Meditation 10 minutes Settling with awareness and stillness Kaya Sthairyam Mindfulness practice (inner silence) Antar Mouna level one Weeks 1-4 Antar Mouna level one Weeks 5-8 Alternate nostril breathing Nadi Shodan [3] Visualisation One-pointed focus-lymph system Dharana [2] Meditation One-pointed focus candle Tratak [3] Weeks 7 and 8 Relaxation-meditation 20 minutes (DVD 10 minutes) Deep relaxation Yoga Nidra [4] Discussion yoga themes 10 minutes Practice in DVD. Full description of each practice: 1. Saraswati, N., Dharana Darshan-Yogic, Tantric and Upanishadic Practices of Concentratrionand Visualization. 2003. Yoga Publications Trust, Munger, Bihar, India. 439. 2. Saraswati, S. Meditations from the Tantras. 2001. Yoga Publications Trust, Munger, Bihar, India. 367. 3. Saraswati, S. Asana, Pranayama, Mudra, Bandha. 1996, Munger, India: Bihar School of Yoga. 543. 4. Saraswati, S. Yoga Nidra. 6th ed. 2006, Munger, India: Bihar School of Yoga. 261. [32], was used. Total QOL was self-recorded with scores related questions. A higher score indicated a lower QOL from 0–10, ten being the best and zero the worst rating rating for that sub-scale. on the day of testing. Sub-scales, each consisting of several questions, for function, symptoms, appearance and emo- Data analysis tions, were also self-recorded. Each question was scaled An a priori sample size calculation was performed and from 1 to 4, four being the worst. The score for each sub- indicated that 19 participants per group would be required scale was based on the mean of the ratings for sub-scale to detect statistically significant changes in the primary Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 5 of 13 http://www.biomedcentral.com/1472-6882/14/214 outcome variables. As the number of participants was and 19 women returned for the week 12 follow up meas- limited by time and other practical constraints, a pilot urement. No women in either group were doing yoga, apart study was conducted. from that prescribed for the intervention group, during the Baseline information between treatment groups for trial, nor had they done it since developing BCRL. demographic and medical characteristics were compared At baseline, the intervention group had a significantly by independent two-tailed t-tests for continuous variables higher BMI (29.1 kg/m ± 4.6; p = 0.023) than the control and by Yates corrected chi-square tests for categorical var- group (25.1 kg/m ± 4.5). There were no other significant iables (SPSS version 19; IBM, Armonk, New York, USA). differences between the intervention and control groups Statistical analyses of outcome measures at baseline and in demographics or medical characteristics at baseline changes between groups at weeks 8 and 12 were performed (Table 2). using STATA statistical software (version 12; STATA Corporation, College Station, Texas, USA). Parametric Outcomes longitudinal data were analysed via mixed methods linear Lymphoedema status regression (ANOVA). Where assumptions of linear re- All participants had been clinically diagnosed with lym- gression were violated, data were analysed using non- phoedema by professional and experienced lymphoedema parametric analysis via ordinal logistic regression. In therapists. We used two methods of measure to determine both methods of analysis, the independent variables were changes in lymphoedema in the trial due to the variance time and group while the dependent variables included that can occur in the definition of lymphoedema and to lymphoedema (L-Dex, arm volume), tissue induration, quantify changes that could occur from the intervention. sensations and quality of life. Post-hoc testing was per- At some measurements some women in both groups may formed on all data using the Holms test to locate the have had variation in lymphoedema status. As this was a means that were significantly different. Statistical signifi- controlled trial we did not account for fluctuation. cance was set at p < 0.05. Due to the low sample size nei- ther multivariate nor covariate analyses were performed. Volume of arm lymphoedema Data is presented as Mean and Standard Deviation unless There was no between group difference in volume of otherwise indicated. arm lymphoedema measured by circumference at base- line. From b-8, there was no significant change between Results groups (Table 3). Participant flow and compliance From 8b-12 (Table 3), there was a significant change The flow of participants through the trial is outlined in between groups in volume of arm lymphoedema (p = Figure 1. Participants in the study were asked at each 0.032) due to the significant increase in the intervention assessment point whether they had experienced any group (25.72 ml; 95% CI: 3.01 to 48.42; p = 0.026). adverse events (pain or abnormal sensation) that might be associated with the intervention. There were no adverse Extra-cellular fluid events attributable to either the yoga or the control inter- There was no between group difference in extra-cellular vention. Two participants withdrew after being diagnosed fluid measured by BIS at baseline. From b-8 and 8b-12 with recurrent cancer during the trial while five others ex- there were no significant changes between groups (Table 3). perienced adverse events requiring their withdrawal from Therefore, this pilot trial was negative with respect to the the study that were unrelated to either their condition or pre-specified primary outcomes. the treatment. Details of these adverse events are included in Figure 1. Tissue induration Due to attrition, fewer participants returned for the There were no between group differences for any meas- week-12 follow-up than completed the week 8 measure- ure of tissue induration of the affected or non-affected ments. Consequently, the results from baseline to end of area measured by tonometry at baseline. From b-8, the 8 week intervention (b-8) and end of the week 8 there was a significant decrease in tissue induration of the intervention to week 12 follow up (8b-12) were analysed affected upper arm in the intervention compared to the separately. Attendance at the group yoga sessions was control group (p = 0.050) (Table 3). From 8b-12, there were high (97%), as was self-reported compliance with the no significant changes in tissue induration between groups. home-practice DVD (86%). Degree of sensations, pain, fatigue and their limiting effects Baseline demographics and medical characteristics There were no between group differences for degree of Twenty-three participants, with a mean age of 57.6 ± sensations, pain, fatigue and their limiting effects measured 10.5 years (range 34–80) and a mean BMI of 27.2 ± 4.9 kg/ by the VAS scale at baseline nor from b-8 or 8b-12 m (range 20.4-37.3), completed the eight week intervention (Table 4). Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 6 of 13 http://www.biomedcentral.com/1472-6882/14/214 Figure 1 Trial flow. Quality of life results of the primary and secondary outcomes. The There were no between group differences for the sub- swelling caused by lymphoedema did not decrease. Eight scales and total QOL score measured by LYMQOL at weeks of yoga resulted in reductions in tissue induration of baseline. From b-8, there was a significant decrease (im- the affected upper arm and in the QOL sub-scale of symp- provement) in the intervention compared to the control toms specific to lymphoedema. However, these improve- group in the QOL sub-scale of symptoms p = 0.038) ments were not sustained at one month post-intervention (Table 5). From 8b-12, there were no significant changes when arm volume of lymphoedema increased. between groups (Table 5). Severity of lymphoedema did not decrease and is com- parable to the response from exercise interventions of Discussion varying durations and modalities for women with BCRL The aim of this small pilot trial was to gain preliminary [12,13,15]. In the current study, L-dex readings from BIS evidence on the effects of an 8-week yoga intervention were virtually unchanged and consistent with those of a on women with stage one BCRL. This paper reports the 12-week combined aerobic and resistance intervention Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 7 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 2 Baseline demographics and medical [11], many of whose participants had low levels of lym- characteristics of the groups phoedema, as in the current trial. In comparison to the Characteristics Intervention Cotnrol P value BIS results, a significant decrease in volume of arm (n = 12) (n = 11) lymphoedema was recorded at week 8 in the interven- Mean ± SD Mean ± SD tion group. While it is possible this result may have Age (years) 55.1 ± 2.5 60.5 ± 3.6 0.230 been affected by a non-significant higher mean arm BMI (kg/m ) 29.1 ± 4.6 25.1 ± 4.5 0.023 volume in theyoga group at baseline (Table3), there- sult is consistent with the volume reduction (p = 0.07) Range 36-65 34-80 found after a four-week daily tai-chi and breathing Number nodes removed 14.3 ± 2.3 11.2 ± 2.7 0.429 intervention [14]. In addition, in our study this result Number of positive nodes 1.5 ± 0.5 3.7 ± 2.3 0.321 was reversed at the week 12 follow-up. These results How long lymphoedema (years) 4.9 ± 1.6 5.1 ± 1.9 0.900 suggest that yoga may be beneficial in reducing or at How long post-surgery 1.2 ± 0.4 1.9 ± 0.7 0.822 least not increasing volume of arm lymphoedema in n(%) n(%) P value women with early-stage BCRL but needs to be ongoing Living arrangements as the benefits may disappear when yoga ceases. The reduction in tissue induration of the affected Live alone 2(14) 3(27) 0.912 upper arm in the intervention group compared to the Live with others 10(83) 8(73) control was a significant beneficial outcome of this trial. Employment The yoga intervention focussed on the repetition and co- Home, retired 5(42) 8(73) 0.280 ordination of physical movements based on range of Employed 7(58) 3(27) motion of the shoulders, spine and whole body, leading Fitness (self-scored) to a gentle, rhythmic stretching and compression of the Low 2(17) 1(9) skin and underlying tissue, particularly in the arms, chest and upper back. Researchers in a tai-chi trial that Medium 8(67) 8(73) 0.913 used a gentle arm opening and closing exercise for women High 2(17) 2(18) with BCRL and reported a significant reduction in the Breast cancer surgery tissue induration of the chest (p = 0.005) [14] suggested Lumpectomy 5(42) 3(27) 0.882 that those actions may have reduced adhesions caused Mastectomy 7(58) 8(73) by fibrosis and improved the quality of the underlying Type of lymph dissection connective tissue. Both the current and the tai-chi trial Sentinel node 0 1(9) 0.980 combined slow physical movement with slow and con- trolled breathing, which also may have created a gentle Axillary clearance 12(100) 10(91) stretching of the connective tissue of the secondary Stage of breast cancer muscles of breathing, such as the pectoral and serratus DCIS 0 1(9) 0.976 anterior muscles, perhaps softening the tissue and enab- 1 3(25) 4(36) ling less restriction of shoulder movement. As stage one 2 6(50) 5(45) lymphoedema may not be accompanied by actual fibrotic 3 3(25) 1(9) tissue [3] we are unable to confirm its use in reducing fi- brotic tissue. However, as fibrosis of tissue is a debilitating Treatment and effects effect of lymphoedema and can increase the possibility of Chemotherapy 8(66) 6(54) 0.867 infection, the outcomes from the tai-chi and the current Effects chemotherapy 7(58) 4(36) 0.525 trial offer preliminary evidence of the beneficial effects of Radiotherapy 9(75) 7(64) 0.890 tai-chi and yoga in softening tissue that warrant further Effects radiotherapy 8(67) 3(27) 0.198 research. Most common area The yoga session offered in this trial consisted not only of radiotherapy of physical practices with focussed awareness on the Chest 7(58) 7(64) 0.909 breath and body, but also specific practices of breathing, Axilla 2(17) 2(18) relaxation and meditation, which are considered effective Axilla and chest 3(25) 2(18) in improving biopsychosocial functioning [33]. The reduc- tion in the LYMQOL sub-scale of symptoms at the comple- Other post-surgery effetcs tion of the yoga intervention is perhaps indicative of the Post-surgery infection 3(25) 3(27) 0.725 holistic beneficial effects of yoga. Symptoms of lymphoe- Post-surgery cording 3(25) 3(27) 0.725 dema adversely affect physical function and QOL in women Post-surgery fluid removal 9(75) 9(82) 0.913 with BCRL [8,34]. A qualitative study into the effect of Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 8 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 3 Results lymphoedema and tissue induration Group mean ± SD b-8 Between group changes 0-8 Group mean ± SD 8b-12 Between group changes 8b-12 Variable Gp(n) Week 0 M ± SD Week 8 M ± SD Δint-Δcon 0–8 MD; (95% Cl) P(0–8) Variable Gp(n) Week 8b M ± SD Week 12 m ± SD Δint-Δcon 8b-12 MD; (95% CI) P(8b-12) Lymphoedema L-dex (BIS) Con (11) 6.49 ± 14.14 7.66 ± 12.64 −1.03; (−4.17 to 2.10) 0.519 Con(10) 8.68 ± 12.83 7.83 ± 13.59 2.57; (−1.04 to 6.18) 0.163 Int(12) 5.89 ± 9.07 6.03 ± 8.24 Int(9) 4.96 ± 6.40 6.67 ± 7.08 Arm volume Con(11) 59.89 ± 78.53 60.75 ± 80.69 −30.28; (−69.33 to 8.78) 0.129 Con(10) 67.65 ± 82.39 58.17 ± 100.42 35.20; (3.09 to 67.32) 0.032 Int(12) 101.45 ± 75.08 72.03 ± 80.77 Int(9) 60.82 ± 82.84 86.53 ± 78.29 Tissue induration (Tonometry) Forearm affected Con(11) 13.96 ± 3.82 14.06 ± 4.80 0-1.89; (−4.88 to 1.16) 0.227 Con(10) 13.65 ± 4.85 12.45 ± 4.36 −0.43; (−2.77 to 1.92) 0.42 Int(12) 15.78 ± 4.79 14.02 ± 3.59 Int(9) 13.87 ± 3.68 12.26 ± 2.41 Forearm non-affected Con(11) 15.61 ± 4.17 15.81 ± 5.20 −140; (−4.59 to 1.78) 0.387 Con(10) 15.37 ± 5.27 12.66 ± 4.00 0.10; (−3.09 to 3.30) 0.95 Int(12) 15.92 ± 5.51 14.72 ± 5.42 Int(9) 14.68 ± 6.23 12.07 ± 4028 Upper arm affected Con(11) 10.66 ± 5.57 12.54 ± 5.91 −3.20; (−641 to 0) 0.050 Con(9) 12.08 ± 6.02 8.92 ± 5.19 0.95; (−1.40 to 3.30) 0.43 Int(12) 11.10 ± 6.09 9.77 ± 3.33 Int(9) 9.63 ± 3.53 7.42 ± 4.39 Upper arm non-affected Con(10) 10.14 ± 4.42 12.05 ± 6026 −2.88; (−5.82 to 0.06) 0.055 Con(10) 11.46 ± 6.34 7.97 ± 5.18 0.53; (−1.98 to 3.03) 0.68 Int(12) 9.88 ± 4.09 8.91 ± 3.621 Int(9) 8.17 ± 3.54 5.21 ± 3.10 Chest affected Con(11) 6.78 ± 2.39 5.53 ± 3.41 −0.36; (−2.63 to 1.91) 0.758 Cont(10Int(9) 5.22 ± 3.43 5.76 ± 1.50 −0.60; (−2.94 to 1.73) 0.61 Int(12) 6.34 ± 2.01 4.73 ± 1.75 4.23 ± 1.14 4.17 ± 1.09 Chest non-affected Con(11) 5.59 ± 1.84 4.76 ± 2.65 −0.34; (−2.85 to 2.17) 0.878 Con(10) 4.70 ± 2.79 6.18 ± 5.00 −1.22; (−5.33 to 2.90) 0.56 Int(12) 6.06 ± 1.87 4.90 ± 1.97 Int(9) 4.98 ± 2.23 5.25 ± 1.60 Upper back affected Con(11) 16.17 ± 2.39 16.76 ± 4.32 0.19; (−3.77 to 4.16) 0.924 Con(10) 16.48 ± 4.45 13.21 ± 5.06 1.10; (−1.51 to 3.70) 0.41 Int(12) 16.06 ± 4.18 16.84 ± 4.82 Int(9) 15.81 ± 4.28 13.63 ± 2.930 Upper back non-affected Con(11) 14.32 ± 3.87 15.13 ± 5.54 −1.42; (−4.85 to 2.02) 0.419 Con(10) 15.04 ± 5.79 14.43 ± 4.32 −0.48; (−3.90 to 2.95) 0.78 Int(12) 15.55 ± 4.21 15.05 ± 4.86 Int(9) 14.66 ± 5.33 13.58 ± 3.83 Δ = change; Gp = Group; M ± SD = Mean ± Standard Deviation; MD = Mean Difference; CI = Confidence Interval. n = number. Con = control group; Int = intervention group. = non-parametic analysis; b = week 0. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 9 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 4 Results sensations, pain, fatigue, and limiting effect of sensations, pain, fatigue VAS Group mean ± SD b-8 Between group changes 0-8 Group mean ± SD 8b-12 Between group changes 8b-12 Variable Gp(n) Week 0 M ± SD Week 8 M ± SD Δint-Δcon 0–8 MD; (95% CI) P(0–8) Variable Gp(n) Week 8b M ± SD Week 12 M ± SD Δint-Δcon 8b-12 MD; (95% CI) P(8b-12) Sensations Con(11) 1.97 ± 1.89 2.01 ± 2.15 −0.55; (02.33 to 1.23) 0.345 Con(10) 2.20 ± 2.17 2.20 ± 2.12 0.30; (−1.21 to 1.81) 0.698 Int(12) 2.39 ± 2.12 1.88 ± 1.83 Int(9) 1.96 ± 1.59 2.26 ± 2.29 Pain Con(11) 1.69 ± 2.31 1.44 ± 2.24 0.06; (−0.74 to 0.87) 0.878 Con(10) 1.57 ± 2.31 1.16 ± 1.48 0.81; (−0.33 to 1.95) 0.165 Int(12) 0.99 ± 1.53 0.80 ± 1.48 Int(9) 1.00 ± 1.67 1.40 ± 1.84 Fatigue † † Con(11) 1.71 ± 2.21 2.06 ± 2.52 −1.05; (−2.50 to 0.41) 0.117 Con(10) 2.26 ± 2.56 1.57 ± 1.54 0.42; (−1.45 to 2.30) 0.551 Int(12) 2.58 ± 2.60 1.88 ± 2.23 Int(9) 2.37 ± 2.50 2.10 ± 1.77 Sensations limit activity Con(11) 1.35 ± 2.81 0.93 ± 1.90 −0.18; (−1.66 to 1.30) 0.793 Con(10) 1.01 ± 1.98 0.8 ± 1.70 0.37; (−0.49 to 1.22) 0.399 Int(12) 1.43 ± 1.76 0.83 ± 0.74 Int(9) 1.20 ± 1.54 1.10 ± 1.54 Pain limit activity Con(11) 0.57 ± 1.10 1.31 ± 2.39 −0.99; (−2.06 to 0.09) 0.362 Con(10) 1.42 ± 2.49 0.89 ± 1.59 0.72; (−0.80 to 2.24) 0.353 Int(12) 0.81 ± 1.44 0.56 ± 0.58 Int(9) 0.61 ± 0.58 0.80 ± 0.93 Fatigue limit activity Con(11) 0.69 ± 1.51 1.34 ± 2.57 −1.0-; (−2.44 to 0.27) 0.315 Con(10) 1.46 ± 2.67 1.07 ± 1.74 0.61; (−0.78 to 2.00) 0.389 Int(12) 1.38 ± 1.85 0.93 ± 0.95 Int(9) 1.03 ± 0.95 1.26 ± 1.24 Δ = change; Gp = Group; M ± SD = Mean ± Standard Deviation; MD = Mean Difference; CI = Confidence Interval; n = number. Con = control group; Int = intervention group. = non-parametric analysis. B = week 0. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 10 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 5 Results total Quality of Life (QOL) and QOL sub-scales QOL Group mean ± SD b-8 Between group changes 0-8 Group mean ± SD 8b-12 Between group changes 8b-12 Variable Gp(n) Week 0 M ± SD Week M ± SD Δint-Δcon 0–8 MD; (95% CI) P(0–8) Variable Gp(n) Week 8b M ± SD Week 12 M ± SD Δint-Δcon 8b-12 MD; (95% CI) p(8b-12) Total QOL Con(11) 7.91 ± 1.22 7.45 ± 1.44 1.04; (−0.19 to 2.26) 0.437 Con(10) 7.40 ± 1.51 7.40 ± 1.51 0.44; (−0.38 to 1.27) 0.290 Int(12) 6.83 ± 2.55 7.42 ± 1.24 Int(9) 7.33 ± 0.87 7.78 ± 1.09 Function Con(11) 1.36 ± 0.40 1.30 ± 0.36 −0.13; (−0.34 to 0.09) 0.364 Cont(10) 1.31 ± 0.38 1.35 ± 0.33 0.13; (−0.07 to 0.33) 0.210 Int(12) 1.48 ± 0.48 1.30 ± 0.31 Int(9) 1.34 ± 0.33 1.51 ± 0.14 Appearance Con(11) 1.56 ± 0.81 1.56 ± 0.86 −0.07; (−0.34 to 0.20) 0.627 Con(10) 1.60 ± 0.69 1.60 ± 0.69 0.10; (−.25 to 0.45) 0.578 Int(11) 1.50 ± 0.34 1.43 ± 0.33 Int(9) 1.42 ± 0.37 1.52 ± 0.37 Symptoms Con(11) 1.69 ± 0.37 1.82 ± 0.54 −0.44; (−0.74 tro −0.13) 0.038 Con(10) 1.90 ± 0.49 1.73 ± 0.47 0.17; (−0.05 to 0.39) 0.124 Int(12) 2.11 ± 0.61 1.81 ± 0.40 Int(9) 1.91 ± 0.38 1.91 ± 0.40 Emotions Con(11) 1.71 ± 0.56 1.61 ± 0.49 −0.18; (−0.62 to 0.26) 0.430 Con(10) 1.62 ± 0.52 1.60 ± 0.56 0.04; (−0.24 to 0.31) 0.801 Int(12) 1.86 ± 0.74 1.58 ± 0.7 Int(9) 1.44 ± 0.45 1.46 ± 0.43 Δ = change; Gp = Group; M ± SD = Mean ± Standard Deviation; MD = Mean Difference; CI = Confidence Interval. N = number. Con = control group; Int = intervention group. = non-parametric analysis. 0 = baseline. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 11 of 13 http://www.biomedcentral.com/1472-6882/14/214 symptoms on the lives of women with BCRL [5] reported whether yoga leads to a decrease in the other QOL that ongoing symptoms continued to cause physical dis- domains. comfort leading to emotional frustration and distress in Physical therapy, as an early intervention, has been spite of treatment to lessen the arm swelling. Moreover, recommended for the prevention or reduction of the persistent symptoms created continual challenges in the morbidity associated with the effects of breast cancer women’s daily life, led to an altered self-image and con- treatment and lymphoedema [9]. The yoga intervention stantly reminded them of the breast cancer experience. In was based on gentle and modified physical movements. the current trial, the degree of sensations, pain and fatigue The benefits gained may indicate that yoga can offer measured separately on the VAS scale did not decrease, another option as an early physical therapy. It may also and yet the QOL sub-scale of symptoms, consisting of a provide an intermediary to more strenuous forms of combination of six different symptoms, improved signifi- exercise and counteract the fear that some women have cantly, indicating a reduction in the adverse effect of in resuming exercise [11,38]. Current best-practice rec- symptoms on women’s QOL. A possible explanation for ommends early intervention to prevent lymphoedema this combination of results could be that the actual symp- becoming worse [39]. That the generally lower levels of toms did not reduce but the women’sreactionto them lymphoedema did not increase in this trial along with did. It is possible that such a finding may be attributable the reduction in tissue induration of the affected upper to the mindful awareness component of yoga, whereby arm, and improvement in the symptoms sub-scale of practitioners learn to witness physical and mental discom- QOL may offer preliminary support that yoga may be a fort without engaging with that discomfort. A study that helpful intervention post-surgery. used yoga as an intervention for women undergoing This trial had several limitations. Women in the current radiotherapy for breast cancer reported a positive cor- trial had been clinically diagnosed with stage one lymphoe- relation between a higher number of intrusive thoughts dema according to the definition from the International and benefit finding from the cancer experience [35]. Society of Lymphology [3], using standardised testing and The researchers suggested this maybearesultofmindful equipment and based on guidelines of the Australasian awareness, in that the intrusive thoughts actually increased, Lymphology Association [27]. However, many of the base- but a negative reaction to the thoughts did not occur. line scores for BIS (L-dex > 10) and volume of arm lym- Symptom management is integral to lymphoedema treat- phoedema (>200 ml) were low and women with higher ment [5,36]. Ridner and colleagues [6] postulated that levels of BCRL may not have experienced similar results. current lymphoedema treatment may not deal adequately Hence a recommendation for future studies would be to with the symptom cluster experienced by women with make an L-dex of >10 or volume of arm lymphoedema BCRL and so complementary therapies may provide other (>200 ml) an additional inclusion criteria and that this management options to reduce the adverse effects com- measure be confirmed by the research team. Furthermore, monly reported. The results of the current trial support fluctuation of levels [7,40] may have occurred in the trial. this postulation. However, it was considered the control group would ac- As other QOL sub-scales did not improve in the count for any factors other than the intervention which current trial, it may be that the reduction in symptoms might be responsible for changes in the outcome variables. precedes the improvement in other QOL domains. As there were no significant within group differences in Comparison with other trials for women with BCRL is the control group for any measure of lymphoedema, difficult, as different QOL tools were used that did not fluctuation of levels seems an unlikely explanation for include a sub-scale of lymphoedema symptoms. Only our results. There were large, albeit non-significant, one yoga trial could be found that reported on symp- mean differences between treatment groups in several toms and QOL ratings. A 12-week yoga intervention for variables at baseline. When baseline results were in- cluded as a covariate for comparison of the two groups women during and after breast cancer treatment, using the Functional Assessment of Cancer Therapy QOL tool, for the primary outcome variables and those for which a found improvements in total QOL and in the social and statistically significant result was observed, this did not affect the significance of the result for the tested variable. emotional QOL sub-scales only in the women not ex- periencing symptoms from chemotherapy [37]. Although As a result, it is unlikely that these imbalances affected the symptoms experienced by women from chemother- changes occurring in the variables during the intervention period. In addition, sample size was small, which was par- apy are different to those from BCRL, it may indicate that symptom amelioration precedes improvement in tially due to all participants starting at the same time and other QOL domains. It would appear that a holistic yoga yoga classes running as a group meaning that additional intervention may be effective in improving symptoms; participants were unable to be recruited to make up for however, a longer intervention with larger numbers is withdrawals and this may have limited some findings. A needed to further test the strength of this hypothesis or post-hoc power calculation has revealed that using this Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 12 of 13 http://www.biomedcentral.com/1472-6882/14/214 study as a pilot for a future study, 179 participants would Acknowledgements This study was supported by grants from the Swan Research Institute (SRI) be required per group aiming to detect a 12% difference in and the Faculty of Health Sciences Seed Funding, UTAS. Equipment was change in lymphoedema between the control and the provided by Flinders University and University of Tasmania. The Women’s intervention groups based on the observed standard devi- Health Centre, Hobart and the Launceston Community Health Centre, Kings Meadows provided venue for conducting the yoga intervention and testing. ation of the between group change as the standard devi- We acknowledge the voluntary provision of professional services in testing ation of the changes was greater than expected. A longer by Marlene Kalis, Christine Lambrechts, Michele Smith, Belinda Mann, Kara intervention may have increased the degree of change or Spaulding, Lara Matuszek and Megan Reid and the professional assistance of Chris Dale and Professor David McNeil. We are indebted to the women of the duration of the beneficial change. Further, the higher Tasmania who volunteered for this trial. BMI of the yoga compared to the control group at base- line may have confounded the results, but due to the small Registration sample size it was thought that covariate analysis using The Australian New Zealand Clinical Trials Registry ACTRN12611000202965. BMI would not produce substantial results. As BMI did Author details not change over the course of the intervention, it was un- Centre for Rural Health, University of Tasmania, Launceston, Australia. 2 3 likely that it affected results. The yoga intervention was School of Medicine, Flinders University, Adelaide, Australia. School of Health Sciences, University of South Australia, Adelaide, Australia. School of based on Satyananda Yoga® using specific practices thought Health Sciences, University of Tasmania, Launceston, Australia. to reduce the effects of lymphoedema and thus the findings may not be generalised to other styles of yoga. Received: 29 July 2013 Accepted: 23 June 2014 Published: 1 July 2014 Conclusion References 1. Australian Institute of Health and Welfare, National Breast and Ovarian The outcomes of this small pilot trial provide preliminary Cancer Centre: Breast Cancer in Australia: An Overview, 2009. Cancer Series no. evidence that an 8-week Satyananda Yoga® intervention, 50, Cat. No. CAN 46. Canberra, ACT, Australia: AIHW; 2009. based on guidelines for exercise and lymphatic drainage 2. National Breast and Ovarian Cancer Centre: Lymphoedema-What you Need to Know. Surry Hills, NSW, Australia: NBOCC; 2008. did not exacerbate lymphoedema measured by arm volume 3. Framework L: Best Practice for the Management of Lymphoedema. MEP Ltd: and extra-cellular fluid and improved tissue induration London, United Kingdom; 2006. of the affected upper arm and the QOL sub-scale of 4. Brennan MJ: Lymphoedema following the surgical treatment of breast cancer: a review of pathophysiology and treatment. J Pain Symptom symptoms. 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Chachaj A, Malyszczak K, Pyszel K, Lukas J, Tarkowski R, Pudelko M, lymphoedema (>200 ml) an additional inclusion criteria Andrzejak R, Szuba A: Physical and psychological impairments of women with upper limb lymphedema following breast cancer treatment. confirmed by the research team. Psychooncology 2010, 19:299–305. 9. Schmitz KH: Balancing lymphedema risk: exercise versus deconditioning Abbreviations for breast cancer survivors. Exerc Sports Sci Rev 2009, 38:17–24. BCRL: Breast cancer-related lymphoedema; QOL: Quality of life. 10. Brown JC, Troxel AB, Schmitz KH: Safety of weightlifting among women with or at risk for breast cancer-related lymphedema: musculoskeletal injuries and health care use in a weightlifting rehabilitation trial. Competing interests Oncologist 2012, 17:112–118. The authors declare that they have no competing interests. 11. Hayes SC, Reul-Hirche HM, Turner J: Exercise and secondary lymphedema: safety, potential benefits, and research-related issues. Med Sci Sports Exerc 2009, 41:483–489. Authors’ contributions 12. McKenzie DC, Kalda AL: Effect of upper extremity exercise on secondary AL conceived the trial and with TB and ADW were responsible for the lymphedema in breast cancer patients: a pilot study. J Clinic Oncol 2003, design of this trial and the construction of the measurement protocol. AL 21:463–466. conducted the yoga intervention. NP was responsible for the design of the 13. Schmitz KH, Ahmed RL, Troxel AB, Cheville A, Smith R, Lewis-Grant L, Bryan lymphoedema methodology. MAI assisted in design of the trial and advice CJ, Williams-Smith CT, Green QP: Weight-lifting in women with breast for the yoga intervention. AL and ADW conducted the statistical analysis. AL cancer-related lymphedema. New Eng J Med 2009, 361:664–673. and ADW drafted and TB, NP, MAI helped draft the manuscript. All authors 14. Moseley AL, Piller NB, Carati CJ: The effect of gentle arm exercise and read and approved the final manuscript. deep breathing on secondary arm lymphedema. Lymphology 2005, 38:136–145. Authors’ information 15. Tidhar D, Katz-Leurer M: Aqua lymphatic therapy in women who suffer AL is a yoga researcher and trains yoga teachers in yoga therapy. TB is from breast cancer treatment-related lymphedema: a randomized Director of Rural Health, University of Tasmania. ADW is a senior lecturer in controlled study. Support Care Cancer 2010, 18:383–392. Clinical Exercise Science, University of Tasmania. NP is Director of the 16. McClure MK, McClure RJ, Day R, Brufsky AM: Randomised controlled trial of lymphoedema clinic at Flinders University. MAI is Director of physical the breast cancer recovery program for women with breast cancer-related movement and yoga researcher at University of South Australia. lymphedema. Am J Occup Ther 2010, 64:59–72. Loudon et al. 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Hayes SC, Johansson K, Stout NL, Prosnitz R, Armer JM, Gabram S, Schmitz Submit your next manuscript to BioMed Central KH: Upper-body morbidity after breast cancer: Incidence and evidence and take full advantage of: for evaluation, prevention, and management within a prospective surveillance model of care. Cancer 2012, 118:2237–2249. 40. Kilbreath SL, Lee MJ, Refshauge KM, Beith JM, Ward LC, Simpson JM, Black • Convenient online submission D: Transient swelling versus lymphoedema in the first year following • Thorough peer review surgery for breast cancer. Support Care Cancer 2013, 21:2207–2215. • No space constraints or color figure charges doi:10.1186/1472-6882-14-214 • Immediate publication on acceptance Cite this article as: Loudon et al.: Yoga management of breast • Inclusion in PubMed, CAS, Scopus and Google Scholar cancer-related lymphoedema: a randomised controlled pilot-trial. BMC Complementary and Alternative Medicine 2014 14:214. • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Complementary Medicine and Therapies Springer Journals

Yoga management of breast cancer-related lymphoedema: a randomised controlled pilot-trial

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Springer Journals
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2014 Loudon et al.; licensee BioMed Central Ltd.
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1472-6882
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Abstract

Background: Secondary arm lymphoedema continues to affect at least 20% of women after treatment for breast cancer requiring lifelong professional treatment and self-management. The holistic practice of yoga may offer benefits as an adjunct self-management option. The aim of this small pilot trial was to gain preliminary data to determine the effect of yoga on women with stage one breast cancer-related lymphoedema (BCRL). This paper reports the results for the primary and secondary outcomes. Methods: Participants were randomised, after baseline testing, to receive either an 8-week yoga intervention (n = 15), consisting of a weekly 90-minute teacher-led class and a 40-minute daily session delivered by DVD, or to a usual care wait-listed control group (n = 13). Primary outcome measures were: arm volume of lymphoedema measured by circumference and extra-cellular fluid measured by bioimpedance spectroscopy. Secondary outcome measures were: tissue induration measured by tonometry; levels of sensations, pain, fatigue, and their limiting effects all measured by a visual analogue scale (VAS) and quality of life based on the Lymphoedema Quality of Life Tool (LYMQOL). Measurements were conducted at baseline, week 8 (post-intervention) and week 12 (four weeks after cessation of the intervention). Results: At week 8, the intervention group had a greater decrease in tissue induration of the affected upper arm compared to the control group (p = 0.050), as well as a greater reduction in the symptom sub-scale for QOL (p = 0.038). There was no difference in arm volume of lymphoedema or extra-cellular fluid between groups at week 8; however, at week 12, arm volume increased more for the intervention group than the control group (p = 0.032). Conclusions: An 8-week yoga intervention reduced tissue induration of the affected upper arm and decreased the QOL sub-scale of symptoms. Arm volume of lymphoedema and extra-cellular fluid did not increase. These benefits did not last on cessation of the intervention when arm volume of lymphoedema increased. Further research trials with a longer duration, higher levels of lymphoedema and larger numbers are warranted before definitive conclusions can be made. Keywords: Yoga, Breast cancer-related lymphoedema, Symptoms, Quality of life, Randomised controlled trial Background As well as fibrosis of the tissue and increased risk of Breast cancer is the second most common form of cancer infection [4], women with BCRL can experience a range in women after skin cancer, and its incidence is expected of debilitating sensations and symptoms [5,6] and in com- to rise due to the ageing population [1]. In spite of parison to women who have had breast cancer treatment improvements to surgical and radiotherapy treatment, without lymphoedema, have impaired physical function at least 20% of treated women will continue to be diagnosed [7] and lower quality of life (QOL) [8]. with breast cancer-related lymphoedema (BCRL) [2] that Due to the multi-dimensional consequences of BCRL, requires lifelong treatment and management [3]. a holistic management approach, including exercise, is recommended [3]. Previously, exercise participation was discouraged due to concerns that exercise may exacerbate the condition; however, there is growing evidence to * Correspondence: Andrew.Williams@utas.edu.au support the use of progressive and supervised exercise School of Health Sciences, University of Tasmania, Launceston, Australia Full list of author information is available at the end of the article © 2014 Loudon et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 2 of 13 http://www.biomedcentral.com/1472-6882/14/214 for women with BCRL with adequate warm-up, cool-down, and data collection sessions were held in Community appropriate rests [9] and suitable training of staff [10]. This Health Centres at two locations, Hobart and Launceston, evidence comes from studies covering a range of exercise between February and May 2011. Both locations consisted modalities, which have reported no increase in severity of an intervention and control group. [11,12] and fewer exacerbations of lymphoedema [13], Randomisation was conducted by a person not associated increased strength [13], reductions in symptoms [13,14], with the trial from a computer-generated random number and improvements in QOL [15,16]. In light of this, re- system (http://www.randomization.com). No stratification search into other holistic interventions, including yoga, occurred. Participants received notification of their group for women with BCRL has been recommended [6,9,14]. allocation in sealed envelopes after baseline testing. Yoga is a holistic system of practices that aims to create balance in the physical, mental and emotional self [17]. It Participants includes breathing (pranayama), postures (asana), medita- Eligibility criteria tion and relaxation. The physical movements and slow Women were eligible for inclusion if they had stage one breathing, which can be adapted to principles of lymphatic unilateral secondary lymphoedema of the arm, as defined clearing, have been used effectively as part of a holistic by the International Society of Lymphology [3] confirmed treatment to reduce lower limb lymphoedema from by a professional lymphoedema therapist, and had com- filariasis [18]. The practices of breathing, meditation pleted treatment for breast cancer (surgery, radiotherapy and relaxation have been reported to improve the psycho- and chemotherapy) at least six months previously, were social functioning of women during and after breast can- over 18 and had sufficient English literacy to provide in- cer treatment [19]. These outcomes may be transferrable formed consent. Briefly, stage one lymphoedema is de- to women with BCRL. Women with BCRL are already fined as early stage lymphoedema that will subside with attending yoga sessions [20], though the outcomes from elevation and may have signs of pitting and was chosen this have not been systematically investigated. for this trial for two principal reasons. Firstly, as this was The aim of this study was to obtain preliminary data the first 8-week pilot trial to use a yoga intervention, to determine the effect of yoga on women with BCRL. women’s safety was paramount and it was thought that This paper reports the results of the primary outcomes lower levels of lymphoedema may be more stable during of lymphoedema status and the secondary outcomes of the intervention period. Secondly, the standard offers a lymphoedema symptoms and QOL in women with stage definition that could be confirmed or negated by a quali- one BCRL. We hypothesised that yoga would reduce fied lymphoedema therapist to account for different swelling caused by lymphoedema relative to usual care methods of clinical measurement. Measurement of and would lead to a reduction in tissue induration and women to confirm lymphoedema status was not possible severity of sensations, pain and fatigue associated with lym- prior to baseline testing because non-metric measurement phoedema and their limiting effects, and improve QOL. equipment was not available to clinicians. Women were excluded if they had recurrent cancer, Methods an infection, were having Complex Lymphoedema Ther- Study design apy, if they were pregnant, wore a pacemaker, which The trial was a multi-centred randomised controlled pilot would affect bioimpedance spectroscopy (BIS) readings, trial using a parallel design with participants allocated to or had severe psychological illness. All participants in intervention or control on a 1:1 allocation ratio. The study the trial received a manual containing information on was registered with the Australian New Zealand Clinical best current care for BCRL. Women were advised not to Trials Registry and ethics approval was granted by the change current exercise nor commence any new activity University of Tasmania’s Social Sciences Human Research during the study period and to seek immediate medical Ethics Committee. This study was part of a larger mixed help if they experienced an exacerbation of lymphoe- methods study. The full protocol has been described pre- dema during the trial. viously [21]. This paper presents the results for the pri- mary outcomes of arm volume of lymphoedema and extra-cellular fluid and the secondary outcomes of tissue Control group induration, sensations and their limiting effects and QOL. Participants randomised to the control group maintained After meeting the selection criteria and giving informed their usual self-care as advised by their lymphoedema consent, participants were randomised to a yoga inter- therapist. Self-care included wearing of compression vention group or a wait-listed usual care control group. sleeves, self-massage, skin protection and continued Outcome measurements were performed at baseline usual lymphatic treatment. The control group were (week 0), week 8 (on completion of intervention) and at offered yoga classes at the completion of the final week 12 (one month after intervention). All intervention measurement. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 3 of 13 http://www.biomedcentral.com/1472-6882/14/214 Yoga intervention group fluid from BIS. These measures can give different outcomes Participants randomised to the intervention group attended [25,26]; for example, BIS results include the fluid in the a weekly 90-minute yoga class taught by an experienced upper part of the arm where it is difficult to get circumfer- and accredited yoga teacher with qualifications in yoga ential readings. therapy and Manual Lymphatic Drainage. Participants were Circumferential readings were taken by a Jobst non- also given a DVD with a 45-minute yoga session and stretch tape according to an established protocol [27] at the instructed to perform it daily. The DVD followed the same metacarpophalangeal joint and at 10 cm intervals from sequence of practices as the class, with fewer postures and the styloid process. Volume of arm lymphoedema was a shorter relaxation. Participants received a logbook in calculated using the truncated cone formula [28] from which they recorded their daily practice along with any the addition of circumferential readings using an Excel relevant comments. Women were given the choice to spreadsheet that compared the affected to the non-affected wear a compression sleeve and, if removed, instructed to arm, resulting in a measure of Absolute Arm Volume be- wear it again immediately after the yoga session [22]. tween the affected and non-affected arm. Measurements The yoga session included documented breathing were recorded in millilitres (ml). practices, physical postures, meditation and relaxation Extra-cellular fluid was measured by BIS L-dex XCA™ techniques according to the Satyananda Yoga® tradition (Bio-Impedimed, Queensland) [29]. Electrodes were placed [23] (Table 1). This style offers systematised practices at anatomical landmarks at the wrist of each arm and right and instruction thought to be suited to women with ankle to provide a low-frequency electrical current. An BCRL. Options for modifications were offered in the increase in extra-cellular fluid is paralleled by a decrease in class and DVD. The practices were chosen to promote impedance and the result recorded as a ratio to the non- lymphatic drainage and to reduce stress and conformed affected arm, taking into consideration arm dominance with exercise guidelines and precautions for women with [26]. The result was an L-dex reading, calculated from soft- BCRL [3,9]. A full rationale for the session and chosen ware provided by the manufacturer. practices has been provided previously [24]. Tissue induration Outcome measures Induration of fibrotic tissue was measured using a digital Measurements, based on validated instruments and pro- tonometer, model 1383 (Biomedical Engineering, Flinders tocols, were taken by trained researchers blinded to the Medical Centre, South Australia) [30]. The digital tonom- group allocation and previous results. Severity of lym- eter measures the resistance to compression in the superfi- phoedema for arm volume and extra-cellular fluid and cial tissues at a given point on the areas of lymph drainage tissue induration were measured by an experienced and (lymphatic territory) [25]. Measurements were taken 10 cm registered lymphoedema physiotherapist at each location. from the cubital fossa on the forearm and 10 cm from the Inter-rater reliability between lymphoedema therapists cubital fossa on the upper arm, in the middle of the areas was assessed pre-trial and rated as acceptable for variabil- of lymphatic territory. Anterior trunk measurements were ity’s between 2-3%. Other trained assessors administered taken at the mid-clavicular line between the second and anthropometric measurements and questionnaires at both third ribs and at the posterior trunk between the acromion places on different days. To ensure consistency at each and the first thoracic rib in the subscapular fossa. Measure- time-point, participants attended at the same time through- ments were taken three times at each position, separated by out the trial and the same assessor was responsible for each a three-second pause, for the affected and non-affected arm measure. Participants were requested to abstain from alco- and trunk. A higher score denoted a higher level of indur- hol for 12 hours and caffeine and exercise for two hours ation of fibrotic tissue. The average of three measurements before testing to increase the validity of the BIS readings. was recorded in millimetres (mm). On arrival at the testing facility, participants underwent anthropometric measurements wearing light clothes and Sensations, pain and fatigue and their limiting effects no footwear. Participants then underwent measures of Participants recorded the severity of sensations, pain and lymphoedema and tissue induration and completed VAS fatigue, and the degree to which sensations, pain and fa- and QOL questionnaires in the same order at each meas- tigue limited activity on the day of measurement on a urement session. 10 cm Visual Analogue Scale (VAS) [31]. A score of 0 cm indicated “no discomfort” and a score of 10 cm indicated Lymphoedema “the worst imaginable”. Lymphoedema was measured with the participant supine and arm dominance noted. Women removed their sleeve Quality of life on entering the measurement venue. Two measures were A validated questionnaire, developed specifically to meas- chosen: arm volume from circumference and extra-cellular ure QOL for people with arm lymphoedema, LYMQOL Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 4 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 1 Yoga session weeks 1–8 including on DVD Practice and time allocated Sanskrit Settling and Breathing 10 minutes (DVD 10 minutes) Settling with awareness Kaya Sthairyam [1] Mindfulness (inner silence) Antar Mouna level one [2] Abdominal, thoracic, clavicular breath Pranayama [3] Full yoga breath Pranayama [3] Postures 35 minutes (DVD 25 minutes) [3] 1a Neck turns Greeva Sanchalana 1b Add outward rotation of opposite arm Utthanpadasana-variation 3 Knee hugs-leg lock pose Supta Pawanmuktasana 4 Shoulder circles Shandha Chakra 5 Bent arm opening, chest towards knees Naukasana-variation combined with Namaskarasana-variation of arms 6 Lying Archer Akarna Dhanurasana-variation 7 Lying rotation Supta Udarakarshanasana-variation 8 Arm/leg stretch Supta Pawanmuktasana 9 Sitting rowing Nauka Sanchalanasana 10 Standing archer Akarna Dhanurasana 11 Modified rope climbing Rajju Karshanasana-variation 12 Modified arm raise, knee bend Tadasana-variation 13 Modified side bend Trikonasana-variation 14 Standing rotation Kati Chakrasana 15 Standing Cat Marjari-asana_variation 16 Modified one legged prayer balance Eka Pada Pranamasana 17 Sitting neck turns Greeva Sanchalana Mindfulness, Pranayama, Meditation 10 minutes Settling with awareness and stillness Kaya Sthairyam Mindfulness practice (inner silence) Antar Mouna level one Weeks 1-4 Antar Mouna level one Weeks 5-8 Alternate nostril breathing Nadi Shodan [3] Visualisation One-pointed focus-lymph system Dharana [2] Meditation One-pointed focus candle Tratak [3] Weeks 7 and 8 Relaxation-meditation 20 minutes (DVD 10 minutes) Deep relaxation Yoga Nidra [4] Discussion yoga themes 10 minutes Practice in DVD. Full description of each practice: 1. Saraswati, N., Dharana Darshan-Yogic, Tantric and Upanishadic Practices of Concentratrionand Visualization. 2003. Yoga Publications Trust, Munger, Bihar, India. 439. 2. Saraswati, S. Meditations from the Tantras. 2001. Yoga Publications Trust, Munger, Bihar, India. 367. 3. Saraswati, S. Asana, Pranayama, Mudra, Bandha. 1996, Munger, India: Bihar School of Yoga. 543. 4. Saraswati, S. Yoga Nidra. 6th ed. 2006, Munger, India: Bihar School of Yoga. 261. [32], was used. Total QOL was self-recorded with scores related questions. A higher score indicated a lower QOL from 0–10, ten being the best and zero the worst rating rating for that sub-scale. on the day of testing. Sub-scales, each consisting of several questions, for function, symptoms, appearance and emo- Data analysis tions, were also self-recorded. Each question was scaled An a priori sample size calculation was performed and from 1 to 4, four being the worst. The score for each sub- indicated that 19 participants per group would be required scale was based on the mean of the ratings for sub-scale to detect statistically significant changes in the primary Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 5 of 13 http://www.biomedcentral.com/1472-6882/14/214 outcome variables. As the number of participants was and 19 women returned for the week 12 follow up meas- limited by time and other practical constraints, a pilot urement. No women in either group were doing yoga, apart study was conducted. from that prescribed for the intervention group, during the Baseline information between treatment groups for trial, nor had they done it since developing BCRL. demographic and medical characteristics were compared At baseline, the intervention group had a significantly by independent two-tailed t-tests for continuous variables higher BMI (29.1 kg/m ± 4.6; p = 0.023) than the control and by Yates corrected chi-square tests for categorical var- group (25.1 kg/m ± 4.5). There were no other significant iables (SPSS version 19; IBM, Armonk, New York, USA). differences between the intervention and control groups Statistical analyses of outcome measures at baseline and in demographics or medical characteristics at baseline changes between groups at weeks 8 and 12 were performed (Table 2). using STATA statistical software (version 12; STATA Corporation, College Station, Texas, USA). Parametric Outcomes longitudinal data were analysed via mixed methods linear Lymphoedema status regression (ANOVA). Where assumptions of linear re- All participants had been clinically diagnosed with lym- gression were violated, data were analysed using non- phoedema by professional and experienced lymphoedema parametric analysis via ordinal logistic regression. In therapists. We used two methods of measure to determine both methods of analysis, the independent variables were changes in lymphoedema in the trial due to the variance time and group while the dependent variables included that can occur in the definition of lymphoedema and to lymphoedema (L-Dex, arm volume), tissue induration, quantify changes that could occur from the intervention. sensations and quality of life. Post-hoc testing was per- At some measurements some women in both groups may formed on all data using the Holms test to locate the have had variation in lymphoedema status. As this was a means that were significantly different. Statistical signifi- controlled trial we did not account for fluctuation. cance was set at p < 0.05. Due to the low sample size nei- ther multivariate nor covariate analyses were performed. Volume of arm lymphoedema Data is presented as Mean and Standard Deviation unless There was no between group difference in volume of otherwise indicated. arm lymphoedema measured by circumference at base- line. From b-8, there was no significant change between Results groups (Table 3). Participant flow and compliance From 8b-12 (Table 3), there was a significant change The flow of participants through the trial is outlined in between groups in volume of arm lymphoedema (p = Figure 1. Participants in the study were asked at each 0.032) due to the significant increase in the intervention assessment point whether they had experienced any group (25.72 ml; 95% CI: 3.01 to 48.42; p = 0.026). adverse events (pain or abnormal sensation) that might be associated with the intervention. There were no adverse Extra-cellular fluid events attributable to either the yoga or the control inter- There was no between group difference in extra-cellular vention. Two participants withdrew after being diagnosed fluid measured by BIS at baseline. From b-8 and 8b-12 with recurrent cancer during the trial while five others ex- there were no significant changes between groups (Table 3). perienced adverse events requiring their withdrawal from Therefore, this pilot trial was negative with respect to the the study that were unrelated to either their condition or pre-specified primary outcomes. the treatment. Details of these adverse events are included in Figure 1. Tissue induration Due to attrition, fewer participants returned for the There were no between group differences for any meas- week-12 follow-up than completed the week 8 measure- ure of tissue induration of the affected or non-affected ments. Consequently, the results from baseline to end of area measured by tonometry at baseline. From b-8, the 8 week intervention (b-8) and end of the week 8 there was a significant decrease in tissue induration of the intervention to week 12 follow up (8b-12) were analysed affected upper arm in the intervention compared to the separately. Attendance at the group yoga sessions was control group (p = 0.050) (Table 3). From 8b-12, there were high (97%), as was self-reported compliance with the no significant changes in tissue induration between groups. home-practice DVD (86%). Degree of sensations, pain, fatigue and their limiting effects Baseline demographics and medical characteristics There were no between group differences for degree of Twenty-three participants, with a mean age of 57.6 ± sensations, pain, fatigue and their limiting effects measured 10.5 years (range 34–80) and a mean BMI of 27.2 ± 4.9 kg/ by the VAS scale at baseline nor from b-8 or 8b-12 m (range 20.4-37.3), completed the eight week intervention (Table 4). Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 6 of 13 http://www.biomedcentral.com/1472-6882/14/214 Figure 1 Trial flow. Quality of life results of the primary and secondary outcomes. The There were no between group differences for the sub- swelling caused by lymphoedema did not decrease. Eight scales and total QOL score measured by LYMQOL at weeks of yoga resulted in reductions in tissue induration of baseline. From b-8, there was a significant decrease (im- the affected upper arm and in the QOL sub-scale of symp- provement) in the intervention compared to the control toms specific to lymphoedema. However, these improve- group in the QOL sub-scale of symptoms p = 0.038) ments were not sustained at one month post-intervention (Table 5). From 8b-12, there were no significant changes when arm volume of lymphoedema increased. between groups (Table 5). Severity of lymphoedema did not decrease and is com- parable to the response from exercise interventions of Discussion varying durations and modalities for women with BCRL The aim of this small pilot trial was to gain preliminary [12,13,15]. In the current study, L-dex readings from BIS evidence on the effects of an 8-week yoga intervention were virtually unchanged and consistent with those of a on women with stage one BCRL. This paper reports the 12-week combined aerobic and resistance intervention Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 7 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 2 Baseline demographics and medical [11], many of whose participants had low levels of lym- characteristics of the groups phoedema, as in the current trial. In comparison to the Characteristics Intervention Cotnrol P value BIS results, a significant decrease in volume of arm (n = 12) (n = 11) lymphoedema was recorded at week 8 in the interven- Mean ± SD Mean ± SD tion group. While it is possible this result may have Age (years) 55.1 ± 2.5 60.5 ± 3.6 0.230 been affected by a non-significant higher mean arm BMI (kg/m ) 29.1 ± 4.6 25.1 ± 4.5 0.023 volume in theyoga group at baseline (Table3), there- sult is consistent with the volume reduction (p = 0.07) Range 36-65 34-80 found after a four-week daily tai-chi and breathing Number nodes removed 14.3 ± 2.3 11.2 ± 2.7 0.429 intervention [14]. In addition, in our study this result Number of positive nodes 1.5 ± 0.5 3.7 ± 2.3 0.321 was reversed at the week 12 follow-up. These results How long lymphoedema (years) 4.9 ± 1.6 5.1 ± 1.9 0.900 suggest that yoga may be beneficial in reducing or at How long post-surgery 1.2 ± 0.4 1.9 ± 0.7 0.822 least not increasing volume of arm lymphoedema in n(%) n(%) P value women with early-stage BCRL but needs to be ongoing Living arrangements as the benefits may disappear when yoga ceases. The reduction in tissue induration of the affected Live alone 2(14) 3(27) 0.912 upper arm in the intervention group compared to the Live with others 10(83) 8(73) control was a significant beneficial outcome of this trial. Employment The yoga intervention focussed on the repetition and co- Home, retired 5(42) 8(73) 0.280 ordination of physical movements based on range of Employed 7(58) 3(27) motion of the shoulders, spine and whole body, leading Fitness (self-scored) to a gentle, rhythmic stretching and compression of the Low 2(17) 1(9) skin and underlying tissue, particularly in the arms, chest and upper back. Researchers in a tai-chi trial that Medium 8(67) 8(73) 0.913 used a gentle arm opening and closing exercise for women High 2(17) 2(18) with BCRL and reported a significant reduction in the Breast cancer surgery tissue induration of the chest (p = 0.005) [14] suggested Lumpectomy 5(42) 3(27) 0.882 that those actions may have reduced adhesions caused Mastectomy 7(58) 8(73) by fibrosis and improved the quality of the underlying Type of lymph dissection connective tissue. Both the current and the tai-chi trial Sentinel node 0 1(9) 0.980 combined slow physical movement with slow and con- trolled breathing, which also may have created a gentle Axillary clearance 12(100) 10(91) stretching of the connective tissue of the secondary Stage of breast cancer muscles of breathing, such as the pectoral and serratus DCIS 0 1(9) 0.976 anterior muscles, perhaps softening the tissue and enab- 1 3(25) 4(36) ling less restriction of shoulder movement. As stage one 2 6(50) 5(45) lymphoedema may not be accompanied by actual fibrotic 3 3(25) 1(9) tissue [3] we are unable to confirm its use in reducing fi- brotic tissue. However, as fibrosis of tissue is a debilitating Treatment and effects effect of lymphoedema and can increase the possibility of Chemotherapy 8(66) 6(54) 0.867 infection, the outcomes from the tai-chi and the current Effects chemotherapy 7(58) 4(36) 0.525 trial offer preliminary evidence of the beneficial effects of Radiotherapy 9(75) 7(64) 0.890 tai-chi and yoga in softening tissue that warrant further Effects radiotherapy 8(67) 3(27) 0.198 research. Most common area The yoga session offered in this trial consisted not only of radiotherapy of physical practices with focussed awareness on the Chest 7(58) 7(64) 0.909 breath and body, but also specific practices of breathing, Axilla 2(17) 2(18) relaxation and meditation, which are considered effective Axilla and chest 3(25) 2(18) in improving biopsychosocial functioning [33]. The reduc- tion in the LYMQOL sub-scale of symptoms at the comple- Other post-surgery effetcs tion of the yoga intervention is perhaps indicative of the Post-surgery infection 3(25) 3(27) 0.725 holistic beneficial effects of yoga. Symptoms of lymphoe- Post-surgery cording 3(25) 3(27) 0.725 dema adversely affect physical function and QOL in women Post-surgery fluid removal 9(75) 9(82) 0.913 with BCRL [8,34]. A qualitative study into the effect of Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 8 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 3 Results lymphoedema and tissue induration Group mean ± SD b-8 Between group changes 0-8 Group mean ± SD 8b-12 Between group changes 8b-12 Variable Gp(n) Week 0 M ± SD Week 8 M ± SD Δint-Δcon 0–8 MD; (95% Cl) P(0–8) Variable Gp(n) Week 8b M ± SD Week 12 m ± SD Δint-Δcon 8b-12 MD; (95% CI) P(8b-12) Lymphoedema L-dex (BIS) Con (11) 6.49 ± 14.14 7.66 ± 12.64 −1.03; (−4.17 to 2.10) 0.519 Con(10) 8.68 ± 12.83 7.83 ± 13.59 2.57; (−1.04 to 6.18) 0.163 Int(12) 5.89 ± 9.07 6.03 ± 8.24 Int(9) 4.96 ± 6.40 6.67 ± 7.08 Arm volume Con(11) 59.89 ± 78.53 60.75 ± 80.69 −30.28; (−69.33 to 8.78) 0.129 Con(10) 67.65 ± 82.39 58.17 ± 100.42 35.20; (3.09 to 67.32) 0.032 Int(12) 101.45 ± 75.08 72.03 ± 80.77 Int(9) 60.82 ± 82.84 86.53 ± 78.29 Tissue induration (Tonometry) Forearm affected Con(11) 13.96 ± 3.82 14.06 ± 4.80 0-1.89; (−4.88 to 1.16) 0.227 Con(10) 13.65 ± 4.85 12.45 ± 4.36 −0.43; (−2.77 to 1.92) 0.42 Int(12) 15.78 ± 4.79 14.02 ± 3.59 Int(9) 13.87 ± 3.68 12.26 ± 2.41 Forearm non-affected Con(11) 15.61 ± 4.17 15.81 ± 5.20 −140; (−4.59 to 1.78) 0.387 Con(10) 15.37 ± 5.27 12.66 ± 4.00 0.10; (−3.09 to 3.30) 0.95 Int(12) 15.92 ± 5.51 14.72 ± 5.42 Int(9) 14.68 ± 6.23 12.07 ± 4028 Upper arm affected Con(11) 10.66 ± 5.57 12.54 ± 5.91 −3.20; (−641 to 0) 0.050 Con(9) 12.08 ± 6.02 8.92 ± 5.19 0.95; (−1.40 to 3.30) 0.43 Int(12) 11.10 ± 6.09 9.77 ± 3.33 Int(9) 9.63 ± 3.53 7.42 ± 4.39 Upper arm non-affected Con(10) 10.14 ± 4.42 12.05 ± 6026 −2.88; (−5.82 to 0.06) 0.055 Con(10) 11.46 ± 6.34 7.97 ± 5.18 0.53; (−1.98 to 3.03) 0.68 Int(12) 9.88 ± 4.09 8.91 ± 3.621 Int(9) 8.17 ± 3.54 5.21 ± 3.10 Chest affected Con(11) 6.78 ± 2.39 5.53 ± 3.41 −0.36; (−2.63 to 1.91) 0.758 Cont(10Int(9) 5.22 ± 3.43 5.76 ± 1.50 −0.60; (−2.94 to 1.73) 0.61 Int(12) 6.34 ± 2.01 4.73 ± 1.75 4.23 ± 1.14 4.17 ± 1.09 Chest non-affected Con(11) 5.59 ± 1.84 4.76 ± 2.65 −0.34; (−2.85 to 2.17) 0.878 Con(10) 4.70 ± 2.79 6.18 ± 5.00 −1.22; (−5.33 to 2.90) 0.56 Int(12) 6.06 ± 1.87 4.90 ± 1.97 Int(9) 4.98 ± 2.23 5.25 ± 1.60 Upper back affected Con(11) 16.17 ± 2.39 16.76 ± 4.32 0.19; (−3.77 to 4.16) 0.924 Con(10) 16.48 ± 4.45 13.21 ± 5.06 1.10; (−1.51 to 3.70) 0.41 Int(12) 16.06 ± 4.18 16.84 ± 4.82 Int(9) 15.81 ± 4.28 13.63 ± 2.930 Upper back non-affected Con(11) 14.32 ± 3.87 15.13 ± 5.54 −1.42; (−4.85 to 2.02) 0.419 Con(10) 15.04 ± 5.79 14.43 ± 4.32 −0.48; (−3.90 to 2.95) 0.78 Int(12) 15.55 ± 4.21 15.05 ± 4.86 Int(9) 14.66 ± 5.33 13.58 ± 3.83 Δ = change; Gp = Group; M ± SD = Mean ± Standard Deviation; MD = Mean Difference; CI = Confidence Interval. n = number. Con = control group; Int = intervention group. = non-parametic analysis; b = week 0. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 9 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 4 Results sensations, pain, fatigue, and limiting effect of sensations, pain, fatigue VAS Group mean ± SD b-8 Between group changes 0-8 Group mean ± SD 8b-12 Between group changes 8b-12 Variable Gp(n) Week 0 M ± SD Week 8 M ± SD Δint-Δcon 0–8 MD; (95% CI) P(0–8) Variable Gp(n) Week 8b M ± SD Week 12 M ± SD Δint-Δcon 8b-12 MD; (95% CI) P(8b-12) Sensations Con(11) 1.97 ± 1.89 2.01 ± 2.15 −0.55; (02.33 to 1.23) 0.345 Con(10) 2.20 ± 2.17 2.20 ± 2.12 0.30; (−1.21 to 1.81) 0.698 Int(12) 2.39 ± 2.12 1.88 ± 1.83 Int(9) 1.96 ± 1.59 2.26 ± 2.29 Pain Con(11) 1.69 ± 2.31 1.44 ± 2.24 0.06; (−0.74 to 0.87) 0.878 Con(10) 1.57 ± 2.31 1.16 ± 1.48 0.81; (−0.33 to 1.95) 0.165 Int(12) 0.99 ± 1.53 0.80 ± 1.48 Int(9) 1.00 ± 1.67 1.40 ± 1.84 Fatigue † † Con(11) 1.71 ± 2.21 2.06 ± 2.52 −1.05; (−2.50 to 0.41) 0.117 Con(10) 2.26 ± 2.56 1.57 ± 1.54 0.42; (−1.45 to 2.30) 0.551 Int(12) 2.58 ± 2.60 1.88 ± 2.23 Int(9) 2.37 ± 2.50 2.10 ± 1.77 Sensations limit activity Con(11) 1.35 ± 2.81 0.93 ± 1.90 −0.18; (−1.66 to 1.30) 0.793 Con(10) 1.01 ± 1.98 0.8 ± 1.70 0.37; (−0.49 to 1.22) 0.399 Int(12) 1.43 ± 1.76 0.83 ± 0.74 Int(9) 1.20 ± 1.54 1.10 ± 1.54 Pain limit activity Con(11) 0.57 ± 1.10 1.31 ± 2.39 −0.99; (−2.06 to 0.09) 0.362 Con(10) 1.42 ± 2.49 0.89 ± 1.59 0.72; (−0.80 to 2.24) 0.353 Int(12) 0.81 ± 1.44 0.56 ± 0.58 Int(9) 0.61 ± 0.58 0.80 ± 0.93 Fatigue limit activity Con(11) 0.69 ± 1.51 1.34 ± 2.57 −1.0-; (−2.44 to 0.27) 0.315 Con(10) 1.46 ± 2.67 1.07 ± 1.74 0.61; (−0.78 to 2.00) 0.389 Int(12) 1.38 ± 1.85 0.93 ± 0.95 Int(9) 1.03 ± 0.95 1.26 ± 1.24 Δ = change; Gp = Group; M ± SD = Mean ± Standard Deviation; MD = Mean Difference; CI = Confidence Interval; n = number. Con = control group; Int = intervention group. = non-parametric analysis. B = week 0. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 10 of 13 http://www.biomedcentral.com/1472-6882/14/214 Table 5 Results total Quality of Life (QOL) and QOL sub-scales QOL Group mean ± SD b-8 Between group changes 0-8 Group mean ± SD 8b-12 Between group changes 8b-12 Variable Gp(n) Week 0 M ± SD Week M ± SD Δint-Δcon 0–8 MD; (95% CI) P(0–8) Variable Gp(n) Week 8b M ± SD Week 12 M ± SD Δint-Δcon 8b-12 MD; (95% CI) p(8b-12) Total QOL Con(11) 7.91 ± 1.22 7.45 ± 1.44 1.04; (−0.19 to 2.26) 0.437 Con(10) 7.40 ± 1.51 7.40 ± 1.51 0.44; (−0.38 to 1.27) 0.290 Int(12) 6.83 ± 2.55 7.42 ± 1.24 Int(9) 7.33 ± 0.87 7.78 ± 1.09 Function Con(11) 1.36 ± 0.40 1.30 ± 0.36 −0.13; (−0.34 to 0.09) 0.364 Cont(10) 1.31 ± 0.38 1.35 ± 0.33 0.13; (−0.07 to 0.33) 0.210 Int(12) 1.48 ± 0.48 1.30 ± 0.31 Int(9) 1.34 ± 0.33 1.51 ± 0.14 Appearance Con(11) 1.56 ± 0.81 1.56 ± 0.86 −0.07; (−0.34 to 0.20) 0.627 Con(10) 1.60 ± 0.69 1.60 ± 0.69 0.10; (−.25 to 0.45) 0.578 Int(11) 1.50 ± 0.34 1.43 ± 0.33 Int(9) 1.42 ± 0.37 1.52 ± 0.37 Symptoms Con(11) 1.69 ± 0.37 1.82 ± 0.54 −0.44; (−0.74 tro −0.13) 0.038 Con(10) 1.90 ± 0.49 1.73 ± 0.47 0.17; (−0.05 to 0.39) 0.124 Int(12) 2.11 ± 0.61 1.81 ± 0.40 Int(9) 1.91 ± 0.38 1.91 ± 0.40 Emotions Con(11) 1.71 ± 0.56 1.61 ± 0.49 −0.18; (−0.62 to 0.26) 0.430 Con(10) 1.62 ± 0.52 1.60 ± 0.56 0.04; (−0.24 to 0.31) 0.801 Int(12) 1.86 ± 0.74 1.58 ± 0.7 Int(9) 1.44 ± 0.45 1.46 ± 0.43 Δ = change; Gp = Group; M ± SD = Mean ± Standard Deviation; MD = Mean Difference; CI = Confidence Interval. N = number. Con = control group; Int = intervention group. = non-parametric analysis. 0 = baseline. Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 11 of 13 http://www.biomedcentral.com/1472-6882/14/214 symptoms on the lives of women with BCRL [5] reported whether yoga leads to a decrease in the other QOL that ongoing symptoms continued to cause physical dis- domains. comfort leading to emotional frustration and distress in Physical therapy, as an early intervention, has been spite of treatment to lessen the arm swelling. Moreover, recommended for the prevention or reduction of the persistent symptoms created continual challenges in the morbidity associated with the effects of breast cancer women’s daily life, led to an altered self-image and con- treatment and lymphoedema [9]. The yoga intervention stantly reminded them of the breast cancer experience. In was based on gentle and modified physical movements. the current trial, the degree of sensations, pain and fatigue The benefits gained may indicate that yoga can offer measured separately on the VAS scale did not decrease, another option as an early physical therapy. It may also and yet the QOL sub-scale of symptoms, consisting of a provide an intermediary to more strenuous forms of combination of six different symptoms, improved signifi- exercise and counteract the fear that some women have cantly, indicating a reduction in the adverse effect of in resuming exercise [11,38]. Current best-practice rec- symptoms on women’s QOL. A possible explanation for ommends early intervention to prevent lymphoedema this combination of results could be that the actual symp- becoming worse [39]. That the generally lower levels of toms did not reduce but the women’sreactionto them lymphoedema did not increase in this trial along with did. It is possible that such a finding may be attributable the reduction in tissue induration of the affected upper to the mindful awareness component of yoga, whereby arm, and improvement in the symptoms sub-scale of practitioners learn to witness physical and mental discom- QOL may offer preliminary support that yoga may be a fort without engaging with that discomfort. A study that helpful intervention post-surgery. used yoga as an intervention for women undergoing This trial had several limitations. Women in the current radiotherapy for breast cancer reported a positive cor- trial had been clinically diagnosed with stage one lymphoe- relation between a higher number of intrusive thoughts dema according to the definition from the International and benefit finding from the cancer experience [35]. Society of Lymphology [3], using standardised testing and The researchers suggested this maybearesultofmindful equipment and based on guidelines of the Australasian awareness, in that the intrusive thoughts actually increased, Lymphology Association [27]. However, many of the base- but a negative reaction to the thoughts did not occur. line scores for BIS (L-dex > 10) and volume of arm lym- Symptom management is integral to lymphoedema treat- phoedema (>200 ml) were low and women with higher ment [5,36]. Ridner and colleagues [6] postulated that levels of BCRL may not have experienced similar results. current lymphoedema treatment may not deal adequately Hence a recommendation for future studies would be to with the symptom cluster experienced by women with make an L-dex of >10 or volume of arm lymphoedema BCRL and so complementary therapies may provide other (>200 ml) an additional inclusion criteria and that this management options to reduce the adverse effects com- measure be confirmed by the research team. Furthermore, monly reported. The results of the current trial support fluctuation of levels [7,40] may have occurred in the trial. this postulation. However, it was considered the control group would ac- As other QOL sub-scales did not improve in the count for any factors other than the intervention which current trial, it may be that the reduction in symptoms might be responsible for changes in the outcome variables. precedes the improvement in other QOL domains. As there were no significant within group differences in Comparison with other trials for women with BCRL is the control group for any measure of lymphoedema, difficult, as different QOL tools were used that did not fluctuation of levels seems an unlikely explanation for include a sub-scale of lymphoedema symptoms. Only our results. There were large, albeit non-significant, one yoga trial could be found that reported on symp- mean differences between treatment groups in several toms and QOL ratings. A 12-week yoga intervention for variables at baseline. When baseline results were in- cluded as a covariate for comparison of the two groups women during and after breast cancer treatment, using the Functional Assessment of Cancer Therapy QOL tool, for the primary outcome variables and those for which a found improvements in total QOL and in the social and statistically significant result was observed, this did not affect the significance of the result for the tested variable. emotional QOL sub-scales only in the women not ex- periencing symptoms from chemotherapy [37]. Although As a result, it is unlikely that these imbalances affected the symptoms experienced by women from chemother- changes occurring in the variables during the intervention period. In addition, sample size was small, which was par- apy are different to those from BCRL, it may indicate that symptom amelioration precedes improvement in tially due to all participants starting at the same time and other QOL domains. It would appear that a holistic yoga yoga classes running as a group meaning that additional intervention may be effective in improving symptoms; participants were unable to be recruited to make up for however, a longer intervention with larger numbers is withdrawals and this may have limited some findings. A needed to further test the strength of this hypothesis or post-hoc power calculation has revealed that using this Loudon et al. BMC Complementary and Alternative Medicine 2014, 14:214 Page 12 of 13 http://www.biomedcentral.com/1472-6882/14/214 study as a pilot for a future study, 179 participants would Acknowledgements This study was supported by grants from the Swan Research Institute (SRI) be required per group aiming to detect a 12% difference in and the Faculty of Health Sciences Seed Funding, UTAS. Equipment was change in lymphoedema between the control and the provided by Flinders University and University of Tasmania. The Women’s intervention groups based on the observed standard devi- Health Centre, Hobart and the Launceston Community Health Centre, Kings Meadows provided venue for conducting the yoga intervention and testing. ation of the between group change as the standard devi- We acknowledge the voluntary provision of professional services in testing ation of the changes was greater than expected. A longer by Marlene Kalis, Christine Lambrechts, Michele Smith, Belinda Mann, Kara intervention may have increased the degree of change or Spaulding, Lara Matuszek and Megan Reid and the professional assistance of Chris Dale and Professor David McNeil. We are indebted to the women of the duration of the beneficial change. Further, the higher Tasmania who volunteered for this trial. BMI of the yoga compared to the control group at base- line may have confounded the results, but due to the small Registration sample size it was thought that covariate analysis using The Australian New Zealand Clinical Trials Registry ACTRN12611000202965. BMI would not produce substantial results. As BMI did Author details not change over the course of the intervention, it was un- Centre for Rural Health, University of Tasmania, Launceston, Australia. 2 3 likely that it affected results. The yoga intervention was School of Medicine, Flinders University, Adelaide, Australia. School of Health Sciences, University of South Australia, Adelaide, Australia. School of based on Satyananda Yoga® using specific practices thought Health Sciences, University of Tasmania, Launceston, Australia. to reduce the effects of lymphoedema and thus the findings may not be generalised to other styles of yoga. Received: 29 July 2013 Accepted: 23 June 2014 Published: 1 July 2014 Conclusion References 1. 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Hayes SC, Johansson K, Stout NL, Prosnitz R, Armer JM, Gabram S, Schmitz Submit your next manuscript to BioMed Central KH: Upper-body morbidity after breast cancer: Incidence and evidence and take full advantage of: for evaluation, prevention, and management within a prospective surveillance model of care. Cancer 2012, 118:2237–2249. 40. Kilbreath SL, Lee MJ, Refshauge KM, Beith JM, Ward LC, Simpson JM, Black • Convenient online submission D: Transient swelling versus lymphoedema in the first year following • Thorough peer review surgery for breast cancer. Support Care Cancer 2013, 21:2207–2215. • No space constraints or color figure charges doi:10.1186/1472-6882-14-214 • Immediate publication on acceptance Cite this article as: Loudon et al.: Yoga management of breast • Inclusion in PubMed, CAS, Scopus and Google Scholar cancer-related lymphoedema: a randomised controlled pilot-trial. 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Journal

BMC Complementary Medicine and TherapiesSpringer Journals

Published: Dec 1, 2014

Keywords: complementary & alternative medicine; internal medicine; chiropractic medicine

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