Physical activity and exercise interventions in women with breast cancer have been reported to improve psychological adjustment, physical functioning, cardiovascular fitness, body composition, and emotional well-being; lower levels of fatigue, depression, anxiety; and help maintain a healthy weight.1–5 Quality of life (QOL) and health-related QOL have been reported to significantly improve after moderate-intensity physical activity,2,4,6–8 and routine physical activity may also translate into survival benefits.9
Breast cancer patients, however, are not routinely receiving recommendations for adopting healthy lifestyle behaviors and cite barriers to exercise such as fatigue, competing daily responsibilities, and scheduling challenges.10,11 However, there is a strong body of evidence from studies with breast cancer survivors on the safety and benefits of routine physical activity after therapy.12 There is a need for comprehensive cancer rehabilitation that addresses physical, psychological, vocational, and social functioning.13 Such rehabilitation programs for survivors should include management of persistent symptoms, prevention of late treatment effects, risk reduction of comorbid illness, and health promotion.13–17 Dissemination of rehabilitation programs to communities where the majority of cancer survivors live and work is an essential component to achieving quality survivorship care.13
This article reports the findings on the feasibility of a community-based exercise intervention and effect on physical and psychological symptoms and QOL in a group of breast cancer survivors. A pilot study was conducted to evaluate the effects of a 3 times per week, 4- to 6-month supervised exercise intervention on bone mass, weight, body composition, physical and psychological symptoms, and QOL. We used a 1-group pretest-posttest design, and participants were recruited through a comprehensive cancer center, private oncology office practices, and notices in community newspapers. Eligible subjects were women diagnosed with stage I or II breast cancer who completed primary and/or adjuvant chemotherapy 36 months or less from the date of enrollment and were either perimenopausal or postmenopausal at time of study entry. Women needed to be English speaking, able to complete questionnaires, able to give informed consent, and be physically able to participate, the latter verified by signed physician approval. The study was approved by the university’s human subject review committee. A detailed description of the study, data analysis, and the findings of the primary outcomes (bone, weight, body composition) have been published.18
The research team partnered with community fitness centers to enhance feasibility and promote a practical approach to exercise adherence by selecting fitness facilities close to where women lived and/or worked. Three fitness centers located in different communities were selected based on their geographic proximity to recruitment patterns of women who qualified as eligible and consented to participate in the study. Fitness centers agreed to allow the research staff to implement the intervention at their center. A dedicated area of the gym was provided with sufficient number of treadmills for the blocks of time scheduled for the study. Participants had fitness center memberships, which were subsidized by the centers in support of the research. A certified master’s-prepared exercise physiologist, a key member of the research team, trained and monitored the study interventionists. The interventionists had various educational preparations in exercise physiology but all had at least 1 basic training certification. The interventionists supervised the participants at each visit in the community fitness centers. Once women agreed to participate and signed consent, exercise schedules were then tailored to participants’ reported availability, and groups were geographically assigned to the most convenient fitness center location. Using the concept of social support, the exercise protocol offered 2-hour blocks of time 5 days a week to promote adherence through participant interaction. The intervention protocol was a progressive aerobic exercise program on a treadmill using a weight belt and a heart rate monitor watch. Target heart rates were calculated for each participant based on clinical data of their resting heart rates taken at baseline visits in the hospital research unit. The intervention included routine stretching exercises, as recommended by the American College Sports Medicine,19 in combination with a standard 5-minute warm-up and cool-down period before and after the time on the treadmill. Because fewer than 25% of the women ever reported having a gym membership before the study, a training session was developed by the research team. The training session included specific components of a stretching program, a description of target heart ranges and the use of the heart rate monitor watch, and the programming of treadmills for safety and protocol progression. Weeks 1 to 4 were dedicated to training weeks, progressing from 10- to 20-minute treadmill sessions 3 times per week to 30 minutes 3 times per week in target heart range of 60% to 65%. From weeks 5 through 16 or 24, women performed 45-minute sessions on the treadmill to achieve a maximal heart rate of 75%. Heart rate monitoring and data collection were conducted simultaneously. Participants reported their heart rates to the interventionist every 5 minutes. Interventionists maintained exercise consistency by adjusting the speed and grade of the treadmills to ensure that participants were in target range during the treadmill sessions. This reporting method kept participants engaged and also provided quality assurance. Details on the weight loading have been previously described.18
Data Collection Procedures
Data were collected at baseline and at 16 and 24 weeks during the participant’s visit at the Yale Center for Clinical Investigation Hospital Research Unit. Demographic data were recorded on an investigator-designed form. Physical and psychological symptom distress and QOL were rated by the participants using the Breast Cancer Prevention Trial Checklist (BCPT), the Symptom Distress Scale (SDS), the Center for Epidemiology Studies–Depression Scale (CES-D), and the Medical Outcomes–Short Form (MOS-SF-36). Medical data were collected from the participant’s outpatient clinic or office record.
The BCPT is a 42-item list of common physical and psychological symptoms.20,21 The respondent is asked if she has been bothered by any of the symptoms over the past 4 weeks, with responses ranging from 0 (not at all) to 4 (extremely). The original instrument indicated a response for the presence of the symptom as yes or no. For this study, 0 indicated the absence of symptom, and severity scores from 1 to 4 indicated presence of the symptom, with distress rated from a little (1) to extremely bothered (4). Exploratory and confirmatory factor analyses have been conducted, with findings suggesting 8 symptom clusters or factor structures, although with minor variation on item loading.21–23 Coefficient α ranged from .55 to .87,23 and discriminate validity was established comparing the BCPT with the MOS-SF-36.22,23
Symptom distress is the perceived discomfort of a symptom by a person, regardless of etiology of the symptom; this was measured using the SDS.24 The instrument consists of 11 symptoms: nausea, pain, fatigue, appetite, concentration, outlook, insomnia, bowel pattern, appearance, breathing, and cough. Two items were added for this study: sexual interest and weight change. Symptom distress is rated on a 5-point scale (1 = mild distress to 5 = very distressful). This instrument has been extensively used in research and has established validity and reliability across 47 studies; internal consistency has been reported to range from 0.70 to 0.92 (R. McCorkle, M. Cooley, J. Shea, unpublished data, 2009).
The CES-D is a 20-item scale designed to assess depressive symptoms.25 Scale scores range from 0 to 60, with higher scores indicating more depressive symptoms. Items are scored on a 4-point scale from 0 (rarely or none of the time) to 3 (most or all of the time). The scale’s reliability and validity are well established.25,26
The MOS-SF-36 is an assessment of self-reported functional ability and has also been conceptualized as a QOL measure. It consists of 8 subscales (physical functioning, role function–physical, bodily pain, social functioning, emotional well-being, role functioning–emotional, energy/fatigue and general health perceptions).27 Each subscale is scored from 0 to 100, with higher scores indicating better functioning. It also provides an overall measure of general health or QOL. Validity and reliability have been established, and internal consistency reliability coefficients have been reported, ranging from 0.62 to 0.96.
Data were entered into an ACCESS database. Analyses were carried out using SAS v 9.2. Instruments were scored in accordance with instructions specific to each instrument. Unless directed differently by scoring instructions, missing values were replaced by mean imputed values across items if 15% or fewer items were missing. Repeated-measures analyses were conducted using mixed modeling; compound symmetry was used to model intraclass correlation. Assumptions of normality and constant standard deviation were assessed. Assumption of normality was marginally violated on some models and was addressed by using transforms.
Thirty-three women consented to participate; 2 never started and 5 women did not complete the study. Of those who failed to complete, 3 dropped out for nonstudy injuries, 1 for a breast cancer recurrence, and 1 for job-related reasons. Of the 26 evaluable women, the mean (SD) age was 51.3 (6.2) years, and most were married, well educated, and employed (Table 1). Initially, the study was funded for 16 weeks, but additional funds were secured, allowing women to continue for a total of 24 weeks. Because of the timing of additional funding, 24 of 26 women were offered extension to 24 weeks of the protocol, and 79.2% (n = 19) accepted. All subjects had completed primary and/or adjuvant chemotherapy for breast cancer and 62% were currently on endocrine therapy with tamoxifen or an aromatase inhibitor (AI). Adherence ranged from 75% to 98%, with an average attendance of 88.2% for all sessions.18
Physical and Psychological Symptom Distress
The 42-item BCPT21–23 was used to identify the prevalence and severity or perceived distress from subjects. At baseline, 15 of the 42 symptoms were reported by 30% or more of the women (range, 30%–85%), with average severity ratings ranging from 1.4 to 2.4 (Table 2). Most of the reported symptoms fell into the general categories of vasomotor symptoms (hot flashes, night sweats, early awakenings), musculoskeletal symptoms (joint pains, aches/pains, muscle stiffness, swelling hands), cognitive changes (difficulty concentrating, forgetfulness), bodily changes (unhappy with appearance, weight gain), and symptoms of atrophic vaginitis (vaginal dryness, dyspareunia). Vasomotor symptoms were the most commonly reported (>50% of subjects) and hot flashes were associated with the highest mean severity ratings, which did not change over time (Table 2). Of the musculoskeletal symptoms, more women reported aches/pains over time, but with lower severity scores, whereas fewer women reported hand swelling, joint pains, and muscle stiffness over time. Muscle stiffness, however, was the only symptom that significantly decreased over time (P = .04). Memory problems were reported more often than problems with concentration, but both cognitive symptoms had relatively low average distress ratings (1.2-1.4). Body image, especially women’s unhappiness with their appearance, was reported by more than 50% of women.
The SDS was used to identify the level of distress associated with 13 symptoms. Of the 13 symptoms, women rated cough, appetite, nausea, bowel, and breathing symptoms as infrequent, not a problem, or very mild distress. The remaining 8 symptoms are depicted in Figure 1 (physical symptoms) and Figure 2 (psychological symptoms). Overall, women reported mild to moderate symptom distress, and distress related to the common symptom of fatigue improved significantly over the course of the exercise intervention (P = .05). There were significant relationships between physical and psychological symptom distress. Fatigue was associated with insomnia (r = 0.42, P = .003), concentration (r = 0.45, P = .001), and outlook toward the future (r = 0.26, P = .03). Distress over weight change was associated with concerns about appearance (r = 0.56, P = .001), a more negative outlook toward the future (r = 0.32, P = .006), and decreased sexual interest (r = 0.32, P = .005).
Depression was measured by the CES-D.25,26 The mean (SD) depression score at baseline was 10.98 (8.58), which significantly decreased at 16 weeks (mean [SD], 7.0 [9.3]; P = .01) and 24 weeks (7.0 [7.7]; P = .08). However, there was no significant change between 16 and 24 weeks, suggesting that the intervention had its effect on mood during the first 16 weeks, which was sustained over time.
Functional Ability and QOL
Physically, women significantly improved over time across the intervention, as measured by the subscales for physical function (P = .03) and vitality (P = .0001) (Table 3). Women also improved in the areas of emotional (P = .02), social functioning (P = .009), and mental health (P = .0005) (Table 3). Overall QOL improved before and after the exercise intervention despite a substantial percentage of women reporting symptoms (Table 2).
In summary, this aerobic exercise intervention over 4 to 6 months in breast cancer survivors resulted in improvements in physical function, fatigue, emotional, and social well-being and overall QOL. Although women commonly reported symptoms, the level of symptom distress reported was in the mild to mild-moderate range. Limitations include the 1-group pretest and posttest design, a volunteer homogenous sample of women, a small sample size, and diversity of time since treatment, although all women were within 2 years of finishing primary or adjuvant chemotherapy and 62% were currently on adjuvant endocrine therapy.18 In a 1-group design, it is unknown if outcomes would have improved with time, as there is no control group. However, this was only a 4- to 6-month intervention, and it is unlikely that specific outcomes, such as physical function, would have improved without the intervention.
Cancer patients transition into survivorship living with persistent physical and psychological symptoms, and many are at risk for late treatment effects and comorbid illness.28 Exercise is perceived as an integral component to cancer rehabilitation for cancer survivors and can improve physical, psychological, and social functioning outcomes.12–15 Women report scheduling problems and managing everyday life as barriers to routine exercise. Exercise programs need to be available in the communities where women live and work to optimize participation, integration into daily life, and a sustained commitment. The YMCA Livestrong program11 is a good example of dissemination of cancer rehabilitation into the community.13 For communities that do not have easy access to the YMCA programs, partnering with physical therapists and fitness centers, especially those with certified cancer personal trainers, are viable options to promote access to structured exercise programs for survivors. Structure, supervision, location, and social support are factors that contribute to the adoption and maintenance of a routine physical activity program.29,30 In the present study, the supportive relationships that the women developed exercising together in the assigned blocks of time may have contributed to the high adherence rates and, possibly, to the QOL outcomes.
The findings from this study demonstrate that adoption of regular exercise by breast cancer survivors in a community setting is feasible, demonstrated by high adherence rates. The findings also suggest that selected symptoms, such as depression and fatigue, improve with exercise. Other symptoms commonly reported by women in the first several years after therapy may or may not be affected by exercise. The symptoms reported by women in this study are similar to other published data that used the BCPT for symptom assessment.31–33 Most women in this study (>80%) reported vasomotor symptoms, but 62% of this sample were on either tamoxifen or an AI. Ganz and colleagues31 reported a 68% incidence of hot flashes among women in the age range of 45 to 51 years, but only 20% of those women were taking tamoxifen, in comparison with a higher incidence (73.5%) reported in a sample of women, of whom 45% were taking tamoxifen.32 There are no known data on the effect of exercise on vasomotor symptoms in breast cancer survivors,1,2 but for postmenopausal women without a cancer diagnosis, the findings are conflicting, ranging from no effect to some decrease in symptoms.34,35 The incidences of vaginal dryness (46%–55%)31,33 and dyspareunia (32%–40%)31–33 were consistent with the experience of the women in this study (Table 2). Musculoskeletal symptoms of joint pains and muscle stiffness were more frequent in this study at baseline (80%) compared with women of similar age but who were not on an AI,31 although these symptoms decreased over time during the exercise intervention. Musculoskeletal symptoms associated with AI therapy are well established and are often a reason for discontinuation. Exercise has been cited as a nonpharmacologic intervention to improve strength and maintain joint mobility but has not been studied related to AI symptom relief.36–38 One study39 used the Western Ontario and MacMaster University Osteoarthritis Index to assess lower extremity join function and pain in a 12-week physical activity intervention in 41 sedentary breast cancer survivors, all of whom were on adjuvant endocrine therapy and, on average, 3 years since surgery. Improvement in joint function in the intervention versus usual care group was reported (P = .05), but there were no significant differences in joint pain or joint stiffness.39
Forgetfulness was reported by 62% to 74% over the 3 time points across the 6 months of this study, which is similar to other published research (62%–79%).31,32 Changes in cognitive function with chemotherapy40 and endocrine therapy41,42 are well established in breast cancer survivors. Exercise as a targeted nonpharmacologic intervention has not been studied for its potential effect on cognitive functioning.43 “Unhappy with appearance” is the BCPT item that addresses body image and was reported by a high percentage of women at baseline (76%), which is consistent with other investigations. Distress ratings for appearance greater than 2.0 was also similarly reported by Alfano and colleagues.32 Body image problems have been associated with type of surgery, chemotherapy side effects (eg, hair loss), weight change, and poorer mental health.44 In this study, the item “unhappy with appearance” was significantly associated with weight change (P = .001). Although this study used aerobic exercise, resistance exercise can improve body composition, even without weight loss, resulting in a potentially better body image.
Depression scores declined significantly over time after the exercise intervention in this study. Duijts and colleagues6 reported an effect size of −0.26 (P = .016) for the effect of exercise on depression, which is consistent with the previously reported effect size of −0.30, although that was not statistically significant (P = .10).2
Fatigue is one of the most common cancer treatment–related symptoms, and there is a large body of research supporting the positive effects of exercise on preventing and/or decreasing the incidence and severity of fatigue,2,45 which supports the proposed relationship of fatigue and exercise.46 As fatigue interferes with everyday function and QOL, exercise should be recommended routinely in practice for all cancer patients, during and after therapy.
Exercise improves QOL,8,47 and the effects are greater with moderate-intensity physical activity over a longer duration.7 In 2 meta-analyses,2,6 statistically significant results were reported for exercise on QOL, with an effect size of 0.29, indicating a small to moderate positive effect. In this study, the MOS-SF-36 was used to measure functional ability and QOL. The 8 subscale scores and the 2 component scale (physical and mental health) scores at baseline were highly consistent, with those reported by others in breast cancer survivors ranging from 6 months to 5 years after treatment.27,48,49 However, the scores in the study reported here all improved after the exercise intervention, and most reached statistical significance (Table 3).
Implications for Practice and Research
The findings from this study confirm that adoption of a routine pattern of exercise is feasible for cancer survivors. However, survivors need explicit prescriptions for health promotion12,13 and strategies to overcome barriers. In addition, the findings provide support for the benefits of exercise on fatigue, depression, and QOL, and as previously reported, exercise maintains weight and bone mass in women who are at otherwise at risk for weight gain and bone loss.18 Combined with the effects of exercise on cardiopulmonary function and the growing evidence to support a potential survival advantage for cancer patients,9 exercise should be included as part of standard care.50 Nurses need to identify community fitness center partners, certified fitness professionals, and physical therapists to work with cancer patients and survivors.12,51 Rehabilitation professionals should be well educated on the sequelae of the various types of cancer treatment so that services can be accurately targeted.12 Health promotion for cancer patients transitioning to survivorship after therapy is completed is an essential nursing responsibility and needs to include information, evidence-based recommendations, and identified resources.
Implications for future research include larger randomized controlled trials with population-based samples to increase generalizability. Longer duration exercise programs monitoring adherence over time, follow-up for sustainability of intervention effects, and exercise interventions with more diverse cancer survivor populations are also needed. It is known that older adults benefit from exercise and there is a gap in our research for the role of exercise in rehabilitation of the older cancer survivor who may also be at greater risk for comorbid health conditions.
We thank Paige Woodward and Daniele Avila for their contributions to the analysis of the QOL data; Marie LaGasse, Barbara Womer, and Linda Dickey-Saucier for their roles as exercise interventionists in the study; and the local community fitness centers who supported the research.
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Keywords:© 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
Cancer rehabilitation; Community; Exercise; Functional ability; Quality of life; Survivorship; Symptoms