Exercise intervention for fatigue-related symptoms in Thai women with breast cancer: A pilot study Wipasiri Naraphong, PhD, RN,1 Adrianne Lane, EdD, RN,2 John Schafer, PhD,2 Kyra Whitmer, PhD, RN2 and Bradley R. A. Wilson PhD3 1
Boromarajonani College of Nursing, Saraburi, Thailand, 2College of Nursing and 3The Health Promotion and Education Program, College of Education, Criminal Justice, and Human Services, University of Cincinnati, Cincinnati, Ohio, USA
The purpose of this pilot study was to preliminarily examine the effects of an exercise program on the symptoms of fatigue, sleep disturbance, mood disturbance, symptom distress, and physical fitness for Thai women with breast cancer. Twenty-three eligible women were randomly assigned to either an experimental group (n = 11) or to a control group (n = 12). Data were collected and analyzed at baseline and again at 4, 7, and 10 weeks. At each time point, fatigue was measured at an expected high point during treatment. Participants in the exercise group demonstrated a trend toward improving the symptoms with mean score changes. Using generalized estimating equations analysis, a significant decrease in mood disturbance was found in the exercise group compared with control at 10 weeks (β = 0.03, P = 0.04). The participants exhibited significantly longer 12-minute walk distance at 10 weeks than those in the control group (t = 2.28, P = 0.04). These results indicate that exercise during adjuvant chemotherapy may be beneficial for Thai women with breast cancer.
INTRODUCTION Breast cancer is burdensome for adult women. It is estimated that 1.7 million women worldwide will be diagnosed with breast cancer in 2020 (Jemal et al., 2011). Breast cancer remains a prominent health concern in Thailand, resulting in both substantial morbidity and mortality for Thai women, the total number of women with newly diagnosed breast cancer makes up 47.8% of all new cancer patients (National Cancer Institute – Thailand, 2011). With advances in cancer treatments, women who have been diagnosed with breast cancer live longer. These treatments may cause serious side-effects which may contribute to multiple symptoms (Bender et al., 2005; Kim et al., 2008). Cancer-related fatigue (CRF) is the most frequent distressing treatment-related symptom reported by cancer patients and it affects their health and well-being across treatment types (Piamjariyakul et al., 2010; Nizamli et al., 2011). The prevalence of CRF increased, ranging from 59 to 100% in patients with breast cancer undergoing adjuvant therapy (Weis, 2011). There is growing body of research that has examined the association between CRF in patients with cancer and multiple symptoms (Beck et al., 2005; Bender
Correspondence address: Wipasiri Naraphong, Nursing Instructor at Boromarajonani College of Nursing, Saraburi, 18/64 Tesaban4 Road, Pakpreaw, Muang, Saraburi 18000, Thailand. Email: [email protected]; [email protected] hotmail.com Received 3 May 2013; revision received 26 October 2013; accepted 3 December 2013
et al., 2005; Kim et al., 2008). Commonly associated with CRF were sleep disturbance, mood disturbance, and symptom distress. These symptoms may increase during treatment and can be significant variables influencing the severity of CRF (Von Ah et al., 2008).
Literature review Numerous studies have demonstrated the benefits of exercise as an effective nonpharmacologic intervention for patients with various kinds of diseases. Walking is the most common exercise described in the literature (Sung & Bae, 2012). Specifically, the results of walking-based exercise studies show alleviation of the symptoms of fatigue and improved psychosocial outcomes in breast cancer patients and survivors (Mock et al., 2005; Rabin et al., 2009). The variability of study outcomes may be attributed to differences in sample characteristics or research designs. Some studies have not shown exercise to yield positive results (Campbell et al., 2005; Payne et al., 2008). The few published home-based exercise studies have managed to agree that breast-cancer patients who exercised regularly at home reported significantly less fatigue during treatment (Schwartz et al., 2001; Mock et al., 2005). However, previous studies have tested exercise interventions to reduce only CRF. Examining one symptom (such as fatigue) in isolation has not adequately allowed oncology nurses or other healthcare providers to determine whether exercise is sufficient to alleviate CRF and other doi: 10.1111/nhs.12124
simultaneously occurring symptoms. Research is needed to explore the efficacy of interventions for multiple symptoms (Barsevick et al., 2010). Few interventional studies on exercise have been done that focus on the Asian cancer population. To our knowledge, there is limited evidence on the effect of exercise in Thai women with breast cancer.Thus, the purpose of this study was to conduct an initial test of the feasibility, and preliminarily examine the effects, of an exercise program on fatigue, sleep disturbance, mood disturbance, and symptom distress.
METHODS Study design This study was a pilot, two-arm, randomized, and controlled trial, which followed women with breast cancer actively receiving adjuvant chemotherapy. All eligible patients participated in a 12-week self-directed exercise program. The baseline assessment and program instructions were given at the first visit when the patients started their adjuvant chemotherapy in the outpatient oncology clinic. The study was also designed to capture the maximal effect of the exercise program on CRF at 48 h, representing an expected time of high fatigue while having treatment. The remaining three measurement points were conducted on the day the patients were scheduled for the subsequent chemotherapy cycles across three weeks: week 4, week 7, and week 10. Data collection points varied only from the due date to three days from the due date for the final three data collection points. The major results were not reported at the end of the 12-week intervention because there was no additional treatment.
uled to receive a minimum of four cycles of each chemotherapy protocol and able to speak, read, and write in Thai. Participants were excluded if they had a history of severe psychiatric illness; had acute or chronic bone, joint, or muscular abnormalities, or used assistive devices for walking as observed during the medical history review and physical examination by an oncologist.
Ethical considerations The study was approved by the Ethics Committee of Lopburi Cancer Center, Thailand, and the Institution Review Board of the University of Cincinnati. The first author (WN), who is fluent in both Thai and English (the bilingual and bicultural principal investigator), was responsible for the management and integrity of the design, intervention implementation, and follow-up of the research project. After determining eligibility, the study purpose and procedures were explained, written consent in Thai was obtained, and all participants were given a copy of the consent form.
Procedures The pilot study was partially blinded. The group allocation was concealed from the patient and the first author until after the completion of the baseline assessments. Participants were randomly assigned to the experimental or attention control group. The eligible consenting participants were placed in order of a table of random assignment provided by the statistician (JS). Participants randomized to the experimental group received the intervention in Thai via an initial, face-to-face, 45-min training session and an exercise kit containing written instructional materials, a pedometer, and exercise logs. The subsequent intervention sessions were scheduled during regular clinic visits. Length of the sessions was tailored to participants’ needs and was about 30–40 min in length. The control group received usual care and weekly telephone calls. Usual care consisted of the typical support and services provided through the cancer center. The healthcare team further provided the participants in the control group with two booklets (general issues about breast cancer and self-care activities for patients receiving chemotherapy) and a Video Compact Disc (self-care activities after breast-cancer surgery). The control group members participated in all data collection assessments but did not receive any study exerciseintervention materials. They also received weekly telephone calls for retention purposes.
The intervention program The intervention was an individually tailored exercise program using progressive exercises to minimize decline in activity during treatment periods. Participants were required to establish frequency and duration goals before their goals were increased from low-intensity to moderate-intensity exercise. Cultural and linguistic factors were considered in design and delivery of the intervention. The culturally
sensitive exercise program (CSEP) was developed to be consistent with clinical practice guidelines (Berger et al., 2010; McNeely & Courneya, 2010). Two components make up the CSEP. First, the CSEP content was organized to give Thai women with breast cancer linguistically and culturally appropriate information. The researchers modified the exercise intervention to be culturally relevant Thai physical activities. These activities were derived from the Compendium of Physical Activities (Ainsworth et al., 2000) and included detailed metabolic equivalents (METs) and descriptions. Participants were asked to choose activities that involved walking on their own and that required low- to moderate-intensity levels (< 3–6 METs) to perform each day for at least 20 min per session (or at least two 10-min sessions to reach a maximum of 20–30 min). The participants were taught to wear a pedometer and increased their total daily steps by 5% over the average number of steps walked weekly during the 12-week intervention period. A family member was invited as a coach to help the participant identify appropriate and safe activities. Second, the program enhanced participant confidence in their ability to successfully start an exercise routine and to improve cardiorespiratory fitness. The participants were instructed and prescribed structured walking on trails in regional parks or temples near their homes with their family members and friends for at least 20–30 min per session (not including the 5 min of warm-up and 5 min of cool-down) or the accumulation of 10-min sessions that will reach a maximum of 20–30 min. Participants were to walk at least three to five days a week at a low to moderate intensity level as measured by the original Borg scale (score 12–14), which is approximately 40–60% of the age-adjusted maximal heart rate. The researcher conducted weekly phone calls for all 12 weeks to monitor exercise participation and to make adjustments to the patient’s walking prescription for the next week as needed.
Data collection All the measures used in the pilot study were available in Thai, and permissions to use these instruments were obtained.
line. The questionnaires collected personal information and information related to disease and treatment.
The Piper Fatigue Scale-Revised The Piper Fatigue Scale-Revised (PFS-R) is a 22-item scale, 0–10 numerical scaling, with four dimensions of fatigue: behavior/severity, affective meaning, sensory, and cognitive/ mood. A total score was obtained by the summation of all 22 items on the PFS-R and division by 22 to keep the score on a 0–10 scaling; the higher the number/score, the worse the fatigue (Piper et al., 1998).The PFS-R has been translated into Thai by Pritsanapanurungsie (2000). This scale has adequate internal consistency among Thai women with breast cancer receiving adjuvant chemotherapy.The Cronbach’s alpha coefficient was 0.95 (Hanprasitkam et al., 2007).
The General Sleep Disturbance The General Sleep Disturbance (GSD) is a 21-item, eightpoint ordinal response scale from 0 (never) to 7 (every day). Concurrent and divergent validity have been reported. After reverse scoring, the mean of all 21 items is calculated (Lee & DeJoseph, 1992). The GSD has been translated into Thai and was used in Thai women with breast cancer receiving adjuvant chemotherapy. The Cronbach’s alpha coefficient was 0.81 (Hanprasitkam et al., 2007).
The Profile of Mood States-Brief Form The Profile of Mood States-Brief Form (POMS-BF) is a 30-item scale, six subscales, 0 (not at all) to 4 (extremely). The POMS-BF has shown adequate content and construct validity (McNair et al., 1992). After reverse scoring, the sum of the six subscales yields a total mood disturbance score: higher scores mean greater mood disturbance. The Thai version of the POMS-BF was used, and demonstrated Cronbach’s alphas ranging from 0.62 to 0.92 for each of the six subscales and 0.93 for the entire scale (Kritpracha, 2004).
The Memorial Symptom Assessment Scale
Intervention feasibility was evaluated by the number of enrolling and retaining participants in the study combined with patient adherence in the exercise group. Adherence refers to weekly average steps walked as recorded on a pedometer (Yamax digiwalker SW-200) throughout the 12-week intervention period. The exercise levels experienced by the participants during structured walking sessions were documented in exercise daily-logs. The 12-min walk test (12MWT) was assessed to compare changes in physical fitness in both groups.
The Memorial Symptom Assessment Scale (MSAS) is a 32-item scale with three subscales: frequency and severity subscales rated on 1 (rarely or slight) to 4 (almost constantly or very severe) and distress subscale rated on 0 (a little bit) to 4 (very much). The Cronbach’s alpha coefficient was 0.83– 0.92. Convergent, discriminant, and construct validity have been reported. Items are scored by summing them in each subscale (e.g., physical, psychological): the higher the score, the more severe, frequent, or distressing the symptoms are for patients (Portenoy et al., 1994). The MSAS has been translated into Thai by Suwisith and colleagues. Cronbach’s alpha coefficient was 0.96 and test-retest reliability ranged from 0.82 to 0.88 among Thai women with breast cancer (Suwisith et al., 2008).
Demographic and medical record questionnaires
The demographic and medical information questionnaires were developed by the researcher and were collected at base-
Data analyses were conducted using IBM SPSS software. Baseline characteristics of the two groups were compared
Mean age Thai Thai Married Divorced/widowed Single ≤ High school ≥ College Currently employed Home maker < $133 $134–400 $401–667 > $667 Never 1 day/week 2–3 days/week 7 days/week MRM Other I II IIIA AC CAF CMF FEC 100 TAC AC + paclitaxel
to-treat” basis, with patients being analyzed in the assigned group (Polit & Gillespie, 2010). However, there was no substantive difference between the models that included and excluded these two participants. No data from the two participants were used in the subsequent GEE modeling analyses.
RESULTS Demographics Twenty-three Thai women with breast cancer participated in the study. The mean age of the participants was 46.78 years (SD = 7.99, range 31–59). They were predominantly diagnosed with breast cancer Stage II (Table 1). Between-group differences were found for education and monthly income. Potential covariates were assessed using both exact methods and the bootstrap followed by a Bonferroni correction with a revised alpha level of 0.0025 (Efron & Tibshirani, 1993). None of the potential covariates achieved statistical
Table 2. Baseline comparison of outcome variables between groups
significance. There were no significant differences between the groups at baseline on any of the outcome variables (Table 2).
Feasibility Regarding intervention feasibility, a total of 177 were initially screened, and 86 patients were potentially eligible. After the principal investigator approached each, 23 individuals were eligible and agreed to participate. Of the 63 individuals remaining, 56 individuals were ineligible (65.12%) and seven refused (23.33%). See Figure 1 for reasons given. Overall retention for the study was 91%. Of the 11 participants who were randomized to the CSEP and adhered to structured walking prescriptions as reported on daily logs, the mean minutes walked per session was 28.53 (SD = 4.49), with a frequency of 3.07 (SD = 2.43) days per week and a mean intensity of 11.78 (SD = 0.94) on the Borg scale. Objective data further supported that the CSEP was feasible by increasing daily steps walked, with a mean increase of 5920 steps (SD = 1523) from baseline to 12-week post-intervention. An independent-sample t test indicated that the 12-MWT was significantly different for participants who completed the study in the exercise group from baseline to week 10 than for those in the attention control group (t = 2.28, P = 0.04).
Effects of the intervention The means and standard deviations of the outcome variables collected during the study period for the exercise and control groups are presented in Table 3. Baseline to 10-week effectsizes were calculated for the effects of the CSEP on the outcome variables. Lower scores on the scales and negative effect-sizes indicate lower levels of CRF and other outcome variables.
Fatigue Participants in the exercise group demonstrated improvements in CRF (Fig. 2), as assessed by the PFS-R, from baseline to the 10-week follow up (d = –0.48). In contrast, the control group exhibited a smaller improvement in CRF from baseline to post-test at week 10 (d = –0.16). The GEE analysis revealed that no significant group or time effects were found in slope differences for CRF (β = –0.00, P = 0.15).
Sleep disturbance Participants in the exercise group show declines in sleep disturbance (Fig. 3), as assessed by the GSD, from baseline to the 10-week follow up (d = 0.30). In contrast, the control group exhibited small improvements in CRF from baseline to post-test at week 10 (d = 0.03). The GEE analysis revealed that no significant group or time effects were found in slope differences for sleep disturbance (β = –0.00, P = 0.35).
Mood disturbance Participants in the exercise group demonstrated an improvement in mood (Fig. 4), as assessed by the POMS-BF, from baseline to the 10-week follow up (d = –0.11). In contrast, the control group exhibited smaller improvements in CRF from baseline to post-test at week 10 (d = 0.01). The GEE analysis indicated that significant slope differences exist between the two groups in mood (β = 0.03, P = 0.04).
Symptom distress Participants in the exercise group demonstrated further improvements in symptom distress (Fig. 5), as assessed by the MSAS, from baseline to the 10-week follow up (d = –0.24). In contrast, the control group exhibited a worsening of symptom distress from baseline to post-test at week 10 (d = 0.63). The GEE analysis indicated that no significant group or time effects were found in slope differences for symptom distress (β = –0.00, P = 0.40).
exercise group had less fatigue than those in the control group over time, but these changes were not large at the end of treatment. The observation supported the majority of previous research that exercise had a beneficial effect on reducing CRF in women with breast cancer during active adjuvant chemotherapy (Mock et al., 2005; Pinto et al., 2005; Wang et al., 2011). This study also offers a new finding that exercise did not worsen CRF at the expected time for the highest level of CRF. Moreover, baseline to 10-week effect-sizes calculated for the effects of CSEP are comparable to those reported in meta-analyses (Brown et al., 2011). In this study a significant reduction in mood disturbance was observed among the exercise participants. However, this effect may not be strong enough to decrease sleep disturbance. These findings are somewhat consistent with previous studies (Chang et al., 2008; Yang et al., 2011). These results suggest that although the CSEP was designed to decrease
Table 3. Mean scores and generalized estimating (GEE) equations analysis of effects of the CSEP based on the groups over time
Figure 2. Changes in mean fatigue scores in the exercise and , Exercise; , Control. control groups.
Figure 3. Changes in mean sleep disturbance scores in the exercise , Exercise; , Control. and control groups.
CRF, these changes may likely be beneficial effects of increased physical activity. This might be explained by the concept of symptom clustering where multiple symptoms can occur concurrently. All symptoms vary in intensity, degree of associated distress, timing, and quality (Barsevick et al., 2006). Comparing this study with previous studies presents a challenge because our method represents a preliminary stage in this field of research. Our investigation focused on measuring the effects of exercise not only on CRF, but multiple
and treatment-related symptoms experienced by women with breast cancer. The findings suggest that nurses should introduce and encourage people with cancer to participate in various kinds of physical activity. The longer people can maintain exercise habits, the greater the overall benefits for symptom relief. Culturally based breast-cancer exercise programs for women can be implemented successfully within the scope of nursing practice. Nursing research should focus on developing tailored interventions that are based on the evaluation of the dose and type of exercise interventions paired with symptom trajectories during chemotherapy.
Mean Mood Disturbance
1.4 1.2 1 0.8 0.6 0.4 0.2
CONCLUSION 0 Baseline
Week 4 Week 7 Time (Weeks)
Figure 4. Changes in mean mood disturbance scores in the exercise , Exercise; , Control. and control groups.
Mean Symptom Distress
The results suggest that Thai women with breast cancer are likely to benefit from a culturally sensitive home-based exercise program. Healthcare professionals should help people establish an exercise habit as early as possible in their cancer trajectory. In a diverse society, the pilot study adds some key directions to the limited body of literature about the delivery of culturally congruent health care in women with different ethnic backgrounds and living with cancer.
A Research Fellowship of the Graduate Student Governance Association, the University of Cincinnati funded travel support for data collection.
1 0.8 0.6
Study Design: WN, AL, JS, KW, BW. Data Collection and Analysis: WN, AL, JS, KW, BW. Manuscript Writing: WN, AL, JS, KW, BW.
0.2 0 Baseline
Week 4 Week 7 Time (Weeks)
Figure 5. Changes in mean symptom distress scores in the exercise , Exercise; , Control. and control groups.
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