Exercise for Breast Cancer Survivors
Research Evidence and Clinical Guidelines
Kerry S. Courneya, PhD
THE PHYSICIAN AND SPORTSMEDICINE - VOL 30 - NO. 8 - AUGUST 2002
In Brief: Exercise can have significant benefits for breast cancer survivors during and after treatment. The general aerobic prescription is for moderate-intensity activity (50% to 75% heart rate reserve), 3 to 5 days per week, 20 to 60 minutes per session. Resistance training should also be incorporated into the programs. Psychological health is optimized by exercise that is enjoyable, develops new skills, incorporates social interaction, and takes place in a mind- and spirit-stimulating environment. Conditions that warrant prescription modification include fatigue and nausea, cytopenias, lymphedema, and bone metastasis. Postcancer exercise is facilitated by instilling a positive attitude toward exercise, confidence in overcoming barriers, and a supportive social environment.
Breast cancer is the most common cancer diagnosed in American women, with approximately 182,800 new cases in 2001.1 Over their lifetime, American women have about a one-in-eight probability of developing the disease, and disease risk increases dramatically with age. Almost 95% of breast cancers are diagnosed in women older than 40. Early detection and improved treatments have resulted in reduced age-adjusted mortality rates over the last decade. Moreover, the current 5-year relative survival rate for breast cancer is about 85%, meaning that most women will live many years after their diagnosis and treatment. Therefore, it behooves physicians to know guidelines and precautions for exercising after breast cancer.
Breast Cancer Therapies and Sequelae
Unfortunately, surviving breast cancer usually means enduring significant and prolonged therapy. Most women with early-stage breast cancer undergo surgical removal of breast tumors and have axillary lymph nodes drained. Many women are then advised to undergo "adjuvant" therapies, primarily radiation, chemotherapy, and hormone therapy. All have related sequelae.
Radiation therapy is used following most breast-conserving surgeries to control local or regional disease, and therapy usually lasts 6 weeks. Treatment may produce some degree of irreversible lung fibrosis. Chemotherapy (eg, antimetabolites, antitubulins, alkylators, or anthracyclines) is used to control suspected micrometastases and typically consists of four to eight cycles of combination chemotherapy over 9 to 21 weeks. Fatigue is common with all of these drugs. Treatment with anthracyclines may cause cardiotoxicity in some patients (<5%). Oral hormone therapy (eg, progestin or antiestrogens such as tamoxifen) is taken daily and may be continued for many years. Premenopausal women may have ovarian ablation; postmenopausal women may take aromatase enzyme inhibitors. These can also cause fatigue and weight gain.
Not surprisingly, breast cancer and its treatments can have negative mental and physical consequences. Emotional effects may include depression, anxiety, stress, poor body image, low self-esteem, loneliness, and loss of a sense of control.2 Physical and functional effects may include asthenia, ataxia, reduced cardiovascular function, muscle weakness and atrophy, difficulty sleeping, fatigue, nausea, vomiting, and pain. Although many of these side effects are common to other cancer patients, breast cancer survivors face additional unique challenges, including limited arm range of motion, lymphedema,3 impaired cognitive function,4 weight gain,5 and osteoporosis.6 Together, these comorbidities can impair a woman's quality of life and suggest a possible therapeutic role for exercise.
Literature Review of Postcancer Exercise
We conducted a literature search in December 2000 of all years and languages using CD-ROM databases (CancerLit, CINAHL, Heracles, Medline, PsycINFO, and SPORT Discus). Key words that related to breast cancer (cancer, oncology, tumor, neoplasm, carcinoma), the postdiagnosis time period (rehabilitation, therapy, adjuvant therapy, treatment, intervention, palliation), and exercise (exercise, physical activity, physical therapy, sport, weight training) were combined and searched. Relevant articles were then examined for further pertinent references.
Included studies had to examine aerobic or resistance exercise training designed to improve cardiovascular function and/or muscular strength. Studies restricted solely to movement therapy or stretching or flexibility exercises for range of motion were excluded. Moreover, studies that did not separate exercise effects from those of a multiple intervention package (eg, exercise combined with diet, social support, psychosocial counseling) were also excluded. The search located 20 studies, 8 of which examined exercise during breast cancer treatment (table 1)7-14 and 12 of which examined exercise after breast cancer treatment (table 2).15-26
|TABLE 1. Results of Exercise During Breast Cancer Treatment|
|Authors||Sample/Treatment||Design||Intervention and Measures||Outcomes and Measures||Results|
|Courneya and Friedenreich7||167 breast cancer survivors who had completed adjuvant therapy||Retrospective||Self-reported mild, moderate, and strenuous exercise during treatment using the Godin Leisure Time Exercise Questionnaire||Quality of life (Functional Assessment of Cancer Therapy and Satisfaction With Life Scale)||Survivors who performed moderate or strenuous exercise during treatment reported highest quality of life|
|Cunningham et al8||66 breast cancer survivors with meta-static disease (mean, 102 mo postdiagnosis) still receiving palliative therapies||Prospective||Self-reported regular exercise (researcher developed)||Survival (medical records)||Survivors who reported regular exercise lived longer than those who did not exercise regularly|
|MacVicar and Winningham9||10 early-stage breast cancer patients on chemotherapy and 6 healthy controls||Pretest-posttest with matched controls (4 non-exercising patients and 6 healthy exercisers)||Supervised cycle ergometer for 10 wk, 3 times/wk, 60% to 85% HRmax||Symptom-limited exercise test and Profile of Mood States||Exercising patients increased functional capacity and mood states equal to that of healthy exercisers; patient controls showed reverse effects|
|MacVicar et al10||45 stage-2 breast cancer patients on chemotherapy||Randomized controlled trial with placebo (stretching) and waiting-list controls||Supervised cycle ergometer for 10 wk, 3 times/wk, 60% to 85% HRreserve||Symptom-limited graded exercise||Exercise group had 40% increase in functional capacity and higher VO2max test time and workload than placebo group or controls|
|Mock et al11||46 early-stage breast cancer patients starting 6 wk of radiation therapy||Randomized controlled trial with usual-care controls||Home-based, self-paced walking for 20-30 min, 4-5 times/wk at 'brisk' intensity for duration of radiation therapy||12-minute walk test, symptom assessment scales, Piper fatigue scale||Exercise group walked farther on the 12-min walk test and had less difficulty, fatigue, anxiety, and body dissatisfaction than the controls|
|Winningham and MacVicar12||42 breast cancer patients 3 to 6 mo into chemotherapy||Randomized controlled trial with placebo (stretching) and waiting-list controls||Supervised cycle ergometer for 10 wk, 3 times/wk, 60% to 85% HRmax||Somatization subscale of the Derogatis Symptom Checklist-90-Revised||Exercise group reported less somatization and nausea than the placebo and controls|
|Winningham et al13||24 stage-2 breast cancer patients 1 to 6 mo into chemotherapy||Randomized controlled trial with wait-list controls||Supervised cycle ergometer for 10-12 wk, 3 times/wk, 20-30 min, 60% to 85% HRmax||Body weight and composition (skinfold calipers)||Exercise group had decreased body fat and increased lean body mass; controls showed opposite effects|
|Schwartz14||27 stage 1 to 3 breast cancer patients starting chemotherapy||Pretest-posttest||Home-based aerobic exercise for 8 wk, 3-4 times/wk, 15-30 min, at low-to-moderate intensity||12-min walk test, Profile of Mood States, Schwartz Cancer Fatigue Scale, and Quality of Life Index for Cancer Patients||Exercise adherents significantly increased walking distance and had significantly less weight gain and decline in quality of life than nonadherents|
|HRmax = maximal heart rate; HRreserve = heart rate reserve|
|TABLE 2. Results of Exercise in Patients After Breast Cancer Treatment|
|Authors||Sample||Design||Intervention and Measures||Outcomes and Measures||Results|
|Baldwin and Courneya15||64 early-stage breast cancer survivors (mean, 51 mo post-diagnosis), most of whom had completed various treatments||Cross-sectional||Self-reported mild, moderate, and strenuous exercise during or after treatment using the Godin Leisure Time Exercise Questionnaire||Self-esteem (Rosenberg Self-Esteem Scale), physical acceptance (Body Image Visual Analogue Scale), physical competence (Physical Self-Efficacy Scale)||Strenuous exercise correlated positively with self-esteem and physical competence|
|Bremer et al16||109 breast cancer survivors (mean, 63.7 mo postdiagnosis) of mixed ethnicity from South Africa who had completed at least surgery||Cross-sectional||Self-reported posttreatment exercise (instrument not reported)||Psychological adjustment (Affect Balance Scale and Index of Well Being), health locus of control (Multidimensional Health Locus of Control Scale)||No differences between survivors who did and did not report a regular exercise program|
|McBride et al17||500 early-stage breast cancer survivors (5-74 mo postdiagnosis) who had completed various treatments||Cross-sectional||Self-reported exercise frequency, duration, length of time, and intentions using a stage-of-change measure||Psychological impact of cancer (Impact of Events Scale)||No differences between survivors who did and did not report regular exercise|
|Nelson18||54 stage-1 breast cancer survivors (9-344 mo postdiagnosis) who had had only surgery||Cross-sectional||Self-reported posttreatment exercise using Health Promoting Lifestyle Profile||Rosenberg Self-Esteem Scale and one-item perceived health scale||Among survivors, health-promoting behaviors (eg, exercise) correlated positively with self-esteem|
|Pinto et al19||71 stage 0 to 2 breast cancer survivors (mean, 8 mo postdiagnosis)||Cross-sectional||Self-reported recent exercise||Mood, coping behaviors, cancer-related symptoms||Exercise related to less confusion, more vigor, and better coping behaviors|
|Young-McCaughan and Sexton20||71 stage 1 or 2 breast cancer survivors (7-80 mo postdiagnosis) who had completed various treatments||Cross-sectional||Self-reported exercise during or after treatment using researcher-developed instrument||Quality of Life Index for Patients With Cancer||Regular exercisers reported a higher quality of life than nonexercisers|
|Harris and Niesen-Vertommen21||20 breast cancer survivors (1-17 yr postdiagnosis) who had received axillary dissection and/or adjuvant therapy||Pretest-posttest||Aerobic and resistance exercise for 8 mo, 3 times/wk, 20-30 min, at moderate intensity||Lymphedema (arm circumference at four locations)||No meaningful change for 99% of the data points, and no difference between ipsilateral and contralateral arms|
|Nieman et al22||12 breast cancer survivors who had completed mixed treatments within the past 4 yr||Randomized, controlled trial with usual care controls||Supervised walking and weight training for 60 min, 3 times/wk at 75% HRmax for 8 wk||Physical functioning (treadmill test, 6-min walk test, leg strength) and natural killer cell activity (NKCA)||Experimental group had increase in 6-min walk test and strength test, decreased heart rate during testing compared with controls; no differences in NKCA|
|Peters et al23 (1994)||24 stage 1 or 2 breast cancer survivors who were at least 6 mo postsurgery||Pretest-posttest||Supervised cycle ergometer program for 5 wk, 5 times/wk, 30-40 min, moderate intensity; then self-reported exercise for 6 mo, 2-3 times/wk, at moderate intensity||Immune (CD 56) and psychological functioning (Freiburg Personality Inventory)||Exercisers had increased NKCA and satisfaction with life|
|Peters et al24(1995)||24 stage 1 or 2 breast cancer survivors who were at least 6 mo postsurgery||Pretest-posttest||Supervised cycle ergometry for 5 wk, 5 times/wk, 30-40 min, at moderate intensity; then self-reported exercise for 6 mo, 2-3 times/wk, at moderate intensity||Immune functioning (number and percentage of granulocytes, lymphocytes, and monocytes)||Exercisers had increased number of granulocytes but decreased number of lymphocytes and monocytes|
|Schulz et al25||28 nonmetastatic breast cancer patients||Pretest-posttest||Supervised exercise 2 times/wk for 10 wk||Physical fitness, anxiety, and depression||Increased physical fitness; decreased anxiety and depression|
|Segar et al26||24 sedentary breast cancer survivors (mean, 42 mo postsurgery)||Randomized controlled trial with waiting-list controls||Unsupervised exercise for 10 wk, 4 times/wk, 30 min, > 60% HRmax controls||Depression (Beck Depression Inventory), anxiety (Spielberger State-Trait Anxiety Inventory), and Rosenberg Self-Esteem Scale||Exercise adherents had reduced anxiety and depression, while controls had no change|
|HRmax = maximal heart rate; HRreserve = heart rate reserve|
Exercise During Breast Cancer Treatment
The studies7-14 that have examined the effects of exercise during breast cancer treatment are not all completely independent. Two studies employed correlational designs, whereas 6 used experimental designs. One of the correlational designs was a retrospective study of 167 breast cancer survivors.7 It revealed that women who performed at least one bout of moderate-to-strenuous exercise during breast cancer treatment reported better posttreatment outcomes, including physical, functional, emotional, and social well-being. The other correlational study8 used a prospective design and reported a serendipitous relationship between postdiagnosis exercise and survival in 66 women with metastatic breast cancer. Although the study was designed to examine the effects of a psychosocial intervention on survival, the only variable that predicted survival was self-reported regular exercise.
Of the 6 experimental studies, 5 examined early-stage breast cancer survivors who received chemotherapy, and 1 examined early-stage breast cancer survivors who received radiation therapy. Study designs consisted of 2 randomized controlled trials with placebo (eg, stretching) and usual-care controls, 2 randomized controlled trials with usual-care controls, 1 pretest-posttest design with 2 matched controls (eg, nonexercising cancer survivors and exercising healthy persons), and 1 pretest-posttest design with no controls. All 6 studies tested an aerobic exercise intervention (4 cycling, 1 walking, and 1 patient-selected) and followed traditional exercise prescription guidelines. Exercise programs ranged from 6 to 12 weeks, and studies examined diverse biopsychosocial outcomes, including functional capacity, body composition, mood states (eg, anxiety, depression), symptoms (eg, nausea, fatigue, sleep disturbances, body dissatisfaction), and general quality of life, but only a few assessed immune responses. All 6 studies showed significant beneficial effects of exercise during treatment in multiple domains of functioning despite modest sample sizes (see table 1).
In general, the studies examining exercise during breast cancer treatment were methodologically sound. Their primary methodologic limitations were: (1) small convenience samples, which restrict the generalizability of the findings, (2) relatively short exercise interventions that did not coincide with the medical treatment in its entirety, and (3) limited follow-up. Moreover, the studies provided very little information on some outcomes important to survivors such as lymphedema prevention, weight gain, cognitive function, and bone loss.
Exercise After Breast Cancer Treatment
Twelve studies have examined posttreatment exercise.15-26 Six studies used correlational designs, and 6 used experimental designs. The 6 correlational studies surveyed early-stage breast cancer survivors (several months to many years postdiagnosis) who had completed one or more treatments (eg, surgery, radiation therapy, chemotherapy). All 6 correlational studies used cross-sectional designs and self-reported measures of exercise. Sample sizes averaged 145 (range, 54 to 500) and focused exclusively on psychosocial outcomes such as self-esteem, body image, perceived competence, mood states (eg, confusion, vigor, anxiety, depression), and general quality of life. Four of the 6 studies found statistically significant associations between exercise and psychosocial outcomes such as physical competence, mood states, self-esteem, and general quality of life (see table 2).
Of the 6 experimental studies, 2 used randomized controlled trial designs with usual-care or waiting-list controls, and 4 used pretest-posttest designs with no controls. All studies followed traditional exercise prescription guidelines in terms of frequency, intensity, and duration, and most exercise programs lasted from 8 to 32 weeks. The most common outcomes studied were biologic (eg, immune system, physical fitness, lymphedema), with lesser attention to psychosocial variables (eg, anxiety, depression, satisfaction with life). Results showed benefits in 2 of the 3 studies examining the immune system, and both studies that assessed physical fitness revealed improvements in patients. The study assessing lymphedema demonstrated that exercise did not increase arm swelling. Finally, the 3 studies that assessed psychosocial outcomes all showed improvements in such measures following the exercise program (see table 2).
Compared with the studies of exercise during breast cancer treatment, those of exercise after treatment were generally less methodologically rigorous. Only 2 of the 12 studies had controls, and 8 of the studies relied on self-reports of exercise. Moreover, the outcomes assessed were more limited in scope, focusing primarily on physiologic changes. Other experimental study limitations included small convenience samples, relatively short exercise interventions, heterogeneous participants (spanning the survivor continuum from several months to many years postdiagnosis), and limited follow-up. Finally, the correlational studies were all cross-sectional rather than prospective.
Overall, despite methodologic limitations, these 20 studies provide evidence that exercise benefits a wide variety of biopsychosocial factors (eg, cardiovascular fitness, body composition, self-esteem, mood states, and fatigue), both during and after breast cancer treatments. In fact, 90% (18/20) of the studies showed beneficial changes in at least one biopsychosocial outcome (or no change in an undesirable outcome in the lymphedema study). Although much more research is needed, it appears that exercise is a useful therapy for most breast cancer survivors.
Guidelines for Prescribing Exercise After Breast Cancer
The 12 intervention studies on postcancer exercise tested an aerobic exercise prescription that mirrors the guidelines recommended by the American College of Sports Medicine (ACSM).27 In brief, each study prescribed 3 to 5 days per week of an aerobic activity (eg, walking, biking) that can be maintained continuously for 20 to 60 minutes at a moderate intensity (60% to 80% maximal heart rate).
These studies have clearly shown that many breast cancer survivors, even during adjuvant therapy, can adhere to a conventional exercise prescription. Moreover, since none of the 12 intervention studies directly compared the relative utility of different exercise prescriptions, researchers cannot say which particular type, frequency, duration, intensity, or rate of progression is best. Clearly, determining the optimal exercise prescription for breast cancer survivors is an important direction for future research. In the meantime, some general guidelines can be applied.
Exercise type. Walking is the natural choice of most survivors and has direct implications for activities of daily living. Cycle ergometry offers advantages that include a sitting position and leg exercise that minimize the effects of ataxia, cognitive impairment, limitations in upper-extremity movement, and arm lymphedema. Any aerobic exercise that meets the ACSM guidelines,27 however, should be feasible after breast cancer.
Upper-body exercises (eg, swimming, rowing, resistance training), it should be noted, are not necessarily contraindicated. Recent research has shown that earlier concerns about vigorous upper-body exercise inducing lymphedema may have been unfounded.21,28 Consequently, breast cancer survivors should be encouraged to follow both an aerobic (table 3) and strength training program (table 4). As a precaution, however, it is recommended that breast cancer survivors wear a compression sleeve on the arm of the affected side during upper-body exercises. Bilaterally affected patients wear sleeves on both arms.
Exercise modifications. The volume of aerobic exercise (ie, frequency, intensity, and duration) can also follow the ACSM guidelines27 but may require modification based on fitness level, comorbid conditions, and tolerance of therapy. High-intensity exercise should probably be avoided during treatments because of the potential immunosuppressive effects29 but is not contraindicated after treatment.
For duration, many researchers have used intermittent training (alternating short bouts of exercise and rest) during chemotherapy treatment as a way of accumulating the recommended 30 minutes.9,11 This approach is recommended for older, deconditioned patients with chronic diseases30,31 and may also be optimal for breast cancer survivors who have been sedentary or are receiving palliative care.
Psychological impact. It is important to recognize that breast cancer survivors exercise as much for psychological health as they do for physical health.32 Therefore, fitness professionals should encourage exercise that is enjoyable, has meaning and purpose, builds confidence, facilitates a sense of control over exercise, develops challenging new skills, incorporates quality social interaction, and takes place in an environment that engages the mind and spirit.
An excellent example of such an exercise program is dragon boat racing (table 5). Dragon boat racing, an ancient Chinese sport, has become popular among breast cancer survivors since the first all-breast-cancer team "Abreast in a Boat" was formed in 1996 by a sport medicine physician and a group of Vancouver women.33 More than 40 dragon boat racing teams exist in Canada,34 with another 25 worldwide organized entirely by other breast cancer survivors. Although workable for some patients, dragon boat racing is not likely feasible for most women with breast cancer, and additional alternatives, like aerobics classes, group circuit training, walking, and swimming, are needed.
Exercise Precautions After Breast Cancer
Besides the general contraindications for any older population,30 additional precautions should be applied to breast cancer survivors (table 6; also see "Coping With Cancer"). Such precautions serve as "red flags" rather than absolute contraindications to exercise. They alert physicians that the risk-to-benefit ratio of exercise may be higher for cancer patients and that close medical supervision may be required. An appropriate exercise prescription can often circumvent the precautionary risks. For example, breast cancer survivors with bone pain or metastases may be advised to swim to reduce the risk of fracture. Similarly, survivors with significant fatigue can do low-to-moderate intensity exercise to reduce the risk of exacerbating their fatigue, while those with ataxia or cognitive impairments should be prescribed exercises with minimal balance and coordination demands (eg, cycle ergometry).
The utility of exercise after breast cancer will depend largely on the motivation and adherence of participants. Long-term adherence to an exercise program is difficult for healthy people, and the challenge is likely heightened after breast cancer. Although evidence has shown that most breast cancer survivors reduce their exercise levels during treatment,7 they can form a very motivated group.35 Nevertheless, having an understanding of the determinants of exercise adherence can help fitness professionals promote exercise for breast cancer survivors.
Ajzen's theory of planned behavior36 is one theoretical model that has been used to understand exercise in breast cancer survivors.32,37 Accordingly, whether or not a woman exercises after breast cancer is strongly influenced by her intention to do so (her level of motivation and willingness to exert effort). Intention, in turn, is thought to be determined by her attitude (positive or negative feelings about exercise), subjective norm for exercise (how she thinks family and friends view her exercising), and her perceived control over exercise (perception of how easy or difficult it will be to carry out).
The key to developing positive attitudes is to highlight the benefits of exercise presented here and to follow the prescription guidelines for optimizing psychological health. To promote a positive subjective norm, it is important to obtain support from the oncologist, family physician, nurse, spouse, family members, friends, and other women with breast cancer. Finally, to facilitate perceptions of control, the woman must have confidence in her ability to exercise in the face of difficult obstacles (eg, fatigue, nausea, lack of knowledge).
The Push to Motivate
Promoting exercise after breast cancer is scientifically justified. Despite some study limitations, results have shown improvements during and after treatment in outcomes that are important to women survivors. Guidelines for aerobic exercise include 3 to 5 days per week at moderate intensity for 20 to 60 minutes in an environment that optimizes psychosocial health. Resistance training should also be an integral part of rehabilitation programs.
Dr Courneya is supported by an Investigator Award from the Canadian Institutes of Health Research and a Research Team Grant from the National Cancer Institute of Canada (NCIC) with funding from the Canadian Cancer Society (CCS) and the CCS/NCIC Sociobehavioral Cancer Research Network. Dr Mackey's research program is supported by the NCIC and the Alberta Cancer Board.
Dr Courneya is a professor in the faculty of physical education and Dr Mackey is an assistant professor in the department of oncology, both at the University of Alberta in Edmonton. Dr McKenzie is a professor in the school of human kinetics at the University of British Columbia in Vancouver, Canada. Address correspondence to Kerry S. Courneya, PhD, Faculty of Physical Education, University of Alberta, E-401 Van Vliet Center, Edmonton, Alberta, T6G 2H9, Canada; e-mail to [email protected].
Disclosure information: Drs Courneya, Mackey, and McKenzie disclose no significant relationship with any manufacturer of any commercial product mentioned in this article. No drug is mentioned in this article for an unlabeled use.