Cancer is a global health burden. In 2007, cancer accounted for 7.6 million deaths worldwide, and this figure is anticipated to rise to 17.5 million by 2050 because of a growing and aging population (2). In the United States alone, almost 1.5 million people are diagnosed with cancer every year and more than 500,000 die from the disease (2). Despite the relatively high mortality rates, the prospects for surviving cancer have improved with an overall 5-yr relative survival rate of about 66% (2). In 2004, there were more than 10 million cancer survivors in the United States alone, representing a fourfold increase in the last 30 yr, and this number is expected to grow. Cancer and its treatments can result in many persisting physical and emotional challenges beyond the formal stage of diagnosis and treatment, placing increasing need for methods to manage treatment side effects and improve quality of life (QoL) (2).
The purpose of this article is to provide an overview and update of research examining the effects of physical activity (PA) upon supportive care and disease end points in cancer survivors. Supportive care end points are primarily indicators of the quality of a cancer survivor's life. QoL encompasses physical, functional, psychological, and social aspects of well-being and includes measures such as generic and disease-specific QoL. Disease end points are primarily indicators of the quantity of expected life, such as disease-free survival, cancer-specific mortality, and overall survival. For this article, a cancer survivor is defined as anyone diagnosed with cancer, from the time of diagnosis and for the balance of life (35). Given the clinical heterogeneity of cancer and its treatments, researchers hypothesize that PA may play a different role at different phases on the cancer continuum. Consequently, we divide our review into PA studies focusing upon (a) supportive care end points during treatment, (b) supportive care end points during survivorship (after treatment), (c) disease end points, and (d) supportive care end points during palliative care. We summarize systematic reviews where available and present recent important studies not included in these systematic reviews.
Physical Activity During Treatment
Numerous systematic reviews on PA in cancer survivors have been published over the past 10 yr with several recent reviews dividing the studies into the treatment and survivorship phases. Conn et al. (4) conducted one of the first metaanalysis studies to examine the separate effects of PA during treatment and after treatment. Twenty-four published and six unpublished studies were included in the review, 13 of which were single-arm, uncontrolled trials. In this review, a medium standardized effect size was reported for physical function, and smaller standardized effect sizes were reported for body composition, mood, QoL, and fatigue. Except for physical function, the pattern of effects suggested more favorable outcomes when interventions were delivered after treatment.
More recently, Schwartz (40) reviewed 34 studies that examined the effects of exercise during treatment and 38 that examined exercise after treatment. During treatment, the literature consistently demonstrated a positive association of PA with improved QoL, cardiorespiratory fitness, muscle strength, flexibility, anxiety, pain, depression, fatigue, and anthropometric measures of body weight, body fat, and other health-related biomarkers. In contrast to Conn's (4) review, the effect of exercise following treatment did not appear to be as strong as during treatment, likely because of the inclusion of observational studies and uncontrolled trials.
The previous reviews did not separate the studies by cancer site, although the majority of studies were in early-stage breast cancer survivors. The extent that we can generalize the effects of interventions across cancer groups is questionable, leading more recent reviews to focus exclusively upon a specific cancer group. McNeely et al. (31) reviewed 14 randomized controlled trials (RCT) examining PA interventions in 717 women diagnosed with stage 0 to III breast cancer. Overall, PA interventions had significant positive and meaningful effects upon QoL, cardiorespiratory fitness, objective physical functioning, and fatigue. Of note, the improvement in fatigue was only statistically significant in the two studies conducted post treatment. No significant change in body weight or body mass index (BMI) were reported in any study; however, when studies assessed body composition with dual x-ray absorptiometry (DEXA), favorable changes were reported for lean body mass and bone density.
Markes and Resch (29) reviewed nine controlled trials investigating PA interventions in 492 women with stages I, II, and III breast cancer receiving adjuvant treatment. The authors concluded that exercise can improve cardiorespiratory fitness significantly with corresponding improvements in activities of daily living; however, there was insufficient evidence for other supportive care outcomes including fatigue, anxiety, depression, immune function, strength, and weight gain. The authors noted considerable heterogeneity between trials for treatment regimens, mode of exercise, and duration of study, which may have resulted in mixed results.
In the first systematic review of PA in prostate cancer (PC) survivors, Thorsen et al. (45) reviewed nine studies examining outcomes of PA interventions, including four RCT, two single-arm trials, and three observational studies. Most studies were conducted with prostate cancer survivors during treatment, in particular androgen deprivation therapy. Despite the limited number of studies and small sample sizes, preliminary findings suggest that PA interventions have beneficial effects upon health outcomes in prostate cancer survivors, especially resistance training. Promising effects of PA were indicated for muscular fitness, physical functioning, fatigue, and health-related QoL.
Liu et al. (27) reviewed 10 PA interventions in patients with hematological cancers (e.g., lymphoma, leukemia, and myeloma) treated with stem cell transplantation. A total of 194 patients participated in these 10 trials, 159 adults and 35 children. Three studies were RCT, one was a nonrandomized controlled trial, and six were uncontrolled trials. Despite heterogeneity and modest methodological quality, encouraging findings were reported for improvement in body composition (lean body weight), muscle strength, aerobic capacity, and fatigue. Overall, Lui et al. (27) concluded that PA interventions are safe and feasible for this population but better quality studies are needed with larger samples, appropriate control groups, and validated outcome measures.
RECENT RANDOMIZED CONTROLLED TRIALS OF PHYSICAL ACTIVITY DURING CANCER TREATMENT
Several recent large randomized exercise trials have been reported since the previously mentioned reviews. Mutrie et al. (34) compared 12 wk of combined aerobic and resistance exercise to usual care in 201 breast cancer patients receiving mixed chemotherapy and/or radiation. Results showed post-intervention effects upon aerobic fitness, shoulder mobility, breast cancer-specific symptoms, depression, and positive mood that largely were maintained at 6-month follow-up.
The largest study of exercise during cancer treatment to date is the Supervised Trial of Aerobic versus Resistance Training (START), a multi-center trial comparing aerobic exercise training and resistance exercise training with usual care in 242 breast cancer patients receiving adjuvant chemotherapy (7). The trial demonstrated that aerobic exercise was superior to usual care for improving self-esteem, aerobic fitness, and percent body fat, whereas resistance training was superior to usual care for improving self-esteem, lower and upper body muscular strength, lean body mass, and chemotherapy completion rate. Improvements in QoL were pronounced particularly for breast cancer patients who preferred and received resistance training, were unmarried, under age 50, received nontaxane chemotherapies, and had more advanced disease stage (8).
In the first trial to compare aerobic and resistance training in prostate cancer survivors, Segal et al. (41) reported findings from an RCT where 121 prostate cancer patients receiving radiation therapy with or without androgen deprivation therapy were randomized to resistance or aerobic exercise or usual care. The findings indicated that both resistance and aerobic exercise mitigated fatigue over the short term (12 wk); however, resistance exercise also resulted in longer-term improvements in fatigue (24 wk) and improved QoL, aerobic fitness, upper and lower body strength and triglycerides, and mitigated increases in body fat. Aerobic training also improved fitness.
The first exercise trial to focus upon adult lymphoma patients was the Healthy Exercise for Lymphoma Patients trial (HELP) (9). In this RCT, 122 lymphoma patients were randomized to usual care or supervised aerobic training for 12 wk. Findings at post-intervention indicated that aerobic exercise was superior to usual care for patient-rated physical function, overall QoL, fatigue, happiness, depression, general health, cardiovascular fitness, and lean body mass. In contrast with results from systematic reviews with breast cancer survivors suggesting larger effects in the postadjuvant setting (4), improvements in the HELP trial were similar in patients off treatment and receiving chemotherapy. Improvements in cardiovascular fitness mediated the improvements in patient-rated physical functioning but not psychosocial functioning. At 6-month follow-up, aerobic exercise training was still superior to usual care for overall QoL, happiness, and depression.
PHYSICAL ACTIVITY DURING SURVIVORSHIP
More than 50% of cancer survivors indicate a preference for beginning PA programs immediately or soon after treatments rather than during (18,23,25,47). This phase therefore represents an important time for intervention. The purpose of PA interventions during the survivorship period is to hasten recovery from the immediate side effects of treatment and prevent any long-term effects. Several metaanalysis studies reviewed earlier observed that the effects of PA interventions may be larger during the survivorship period compared with the treatment period (4,31). Since the publication of these reviews, several studies explicitly have targeted the survivorship phase and reported beneficial effects of PA upon supportive care outcomes.
Daley et al. (10) compared the effects of 8 wk of either aerobic exercise or flexibility exercise to usual care in 108 breast cancer survivors, 12-36 months post-treatment. Beneficial post-intervention effects were reported for QoL, fatigue, self-worth, aerobic fitness, and depression with the effect upon depression being maintained at 6-month follow-up.
The Weight Training for Breast Cancer Survivors (WTBS) study examined the effects of twice weekly weight training on supportive care outcomes in 86 breast cancer survivors 4-36 months post-treatment (36). The results indicated that weight training had beneficial effects upon physical and psychosocial QoL scores, and improvements were associated with increases in lean body mass and upper body strength. There were no changes in depressive scores.
The ACTivity PromoTION (ACTION) trial (48) was an RCT designed to determine the effects of breast cancer-specific print materials, a step pedometer, or their combination upon PA and health-related QoL in breast cancer survivors, compared with a control group receiving a standard PA recommendation. At 3 months post-intervention, breast cancer-specific print materials and pedometers were effective in increasing PA and health-related QoL (HRQOL). Specifically, moderate to vigorous intensity PA increased by approximately 40-60 min·wk−1 in the intervention group compared with controls, and brisk walking increased by 60-90 min·wk−1. The combined group also reported significantly better HRQOL and reduced fatigue compared with the standard control group.
Similar to the treatment phase, the majority of RCT during the survivorship phase have been limited to a few cancer survivor groups, predominantly breast cancer survivors. One exception is a study by von Gruenigen et al. (49) that assessed the feasibility of a lifestyle intervention program for promoting weight loss and increased PA in obese endometrial cancer survivors. Early stage (stage I to II) endometrial cancer survivors were randomized to a 6-month lifestyle program or usual care condition. The lifestyle group received group and individual counseling for 6 months. At 12 months, the lifestyle group lost 3.5 kg compared to a 1.4 kg gain in the control group. Moreover, women in the lifestyle group demonstrated significant improvements in PA compared with usual care participants. Of note, weight loss was maintained 6 months after completion of the intervention. This study provides feasibility of conducting a weight loss intervention in obese endometrial cancer survivors.
Several observational studies using cross-sectional designs have examined the association between PA and QoL in understudied cancer survivor groups. These studies have reported positive associations between PA and QoL in multiple myeloma (19), brain (21), ovarian (43), endometrial (6), bladder (24), colorectal (28,38), lung (20), and non-Hodgkins lymphoma (46,3) cancer survivors, but randomized controlled trials are needed in these diverse populations.
PHYSICAL ACTIVITY AND DISEASE END POINTS
Perhaps the most compelling question in this area of research is whether PA can reduce the risk of disease recurrence and extend survival. Until recently, research studies on PA in cancer survivors have focused predominantly upon supportive care end points. Within the last decade, several recent large epidemiologic studies have examined the association between both prediagnosis PA (1,12,13) and postdiagnosis PA (16,17,32,33,42) with disease end points in breast and colon cancer survivors. There are no systematic reviews of PA and cancer prognosis; consequently, we review several of the key studies on this topic here.
The majority of studies have examined the association between PA and breast cancer outcomes. In the Nurses Health Study, Holmes et al. (17) followed 2987 women diagnosed with stage I to III breast cancer for a median of 8 yr. After adjusting for known prognostic factors, including BMI, women who participated in at least 9 MET·h·wk−1 of PA had a 25% to 50% risk reduction in recurrence, breast cancer mortality, and all-cause mortality. This association was particularly apparent in women with hormone-responsive tumors.
Holick et al. (16) followed 4482 breast cancer survivors enrolled in the Collaborative Women's Longevity study to examine the association between postdiagnosis recreational PA and risk of breast cancer mortality over 6 yr. Results indicated that women engaging in higher PA had a lower risk of breast cancer death and all-cause death by 40% to 50%. The association remained after adjusting for known prognostic factors including age, family history of breast cancer, disease stage, treatments, energy intake, and BMI.
Sternfeld et al. (42) reported findings from the Life After Cancer Epidemiological study (LACE), a prospective investigation of behavioral risk factors, and health outcomes in 1970 women diagnosed with early breast cancer. This is the first study to encompass both recreational and non-recreational PA. In this analysis, only all-cause mortality risk significantly declined as moderate intensity PA increased. Moreover, subgroup analysis suggested that the trend for reduced risk of all-cause mortality was significant in postmenopausal women only and estrogen/progesterone status at time of diagnosis. In addition, risk was reduced for normal weight women, not for overweight or obese women. In contrast with moderate PA, the risk estimates associated with vigorous activity showed little or no evidence of a protective association for any outcome, including all-cause mortality.
Two observational studies have examined the association between PA and colorectal cancer outcomes. Meyerhardt et al. (32) examined the association between PA prediagnosis (median 6 months) and postdiagnosis (median 22 months), and risk of colorectal specific mortality and all-cause mortality in 573 women from the Nurses' Health Study diagnosed with stage I to III colorectal cancer. A significant negative linear association was reported between postdiagnosis PA and risk of cancer specific and overall mortality. The association remained after adjustment for known prognostic factors, including BMI. Similarly, in a companion study, Meyerhardt et al. (33) reported a significant negative linear association between PA and disease-free survival, recurrence-free survival, and overall mortality in 832 patients with stage III colon cancer.
Overall, research suggests that PA is associated with a lower risk of disease recurrence and longer survival in breast and colon cancer survivors. Nevertheless, all of the studies to date are based upon observational data. The Colon Health and Life-Long Exercise Change (CHALLENGE) trial is a multi-center randomized trial designed to determine the effects of a 3-yr structured PA intervention upon disease outcomes in stage II and III colon cancer survivors who have completed adjuvant therapy within the previous 2-6 months (5). An estimated 962 colon cancer survivors will be assigned randomly to a structured PA intervention or to general health education materials. The primary end point is disease-free survival, and secondary end points will include patient-reported outcomes, objective physical functioning, biologic correlative markers, and an economic analysis. If this research confirms that PA improves disease-free survival in colon cancer survivors, then programs and policies to promote such activity for this purpose may be adopted and tested with other cancer survivor groups (5).
PHYSICAL ACTIVITY DURING PALLIATIVE CARE
Despite the improvements in treatment and survival, approximately two thirds of individuals diagnosed with cancer are not cured of the disease, and about half will eventually die from the disease (44). Based on the number of cancer deaths per year, and a growing and aging population, the demand for palliative care is likely to dramatically increase in coming years (50). The goal of palliative cancer care is to help advanced cancer patients maximize their quality of life by management of cancer-related symptoms (50). The ability to maintain physical independence and perform self-care activities can have a profound impact upon quality of life. It stands to reason therefore that supportive care interventions that maintain a patient's mobility for as long as possible have the potential to improve advanced cancer patients' QoL significantly (22).
Lowe et al. (26) have reported the first systematic review of PA as a supportive care intervention in palliative cancer patients. They found six studies that were largely pilot and case studies focusing upon feasibility issues such as recruitment and adherence, emphasizing this new emerging field. The sole randomized controlled trial (15) showed a statistically significant slower rate of decline in total well-being and total fatigue between treatment and control groups, and the two single-arm trials demonstrated trends of improvement in QoL, fatigue, and physical function (37,39). The three case studies likewise showed improvement in selected outcomes. Overall, there is preliminary evidence that at least some advanced cancer patients are willing and able to participate in PA interventions and that such interventions can impact positively upon QoL. However, the paucity of evidence and heterogeneity between studies precludes definitive conclusions for the efficacy of physical activity as a supportive care intervention in palliative patients.
Overall, research indicates that PA is safe and feasible for several cancer survivor groups and results in favorable improvements in QoL, physical function, and psychosocial outcomes. Advances in the field are reflected by reviews separating different phases of the cancer continuum, cancer groups, specific symptoms, and the emergence of several large scale multi-center trials. Nevertheless, there is a need for more methodologically rigorous studies with large sample sizes, in particular among understudied cancer groups. The studies reviewed emphasize the heterogeneity between studies and the heterogeneous response both between and within cancer groups. Larger sample sizes would enable subgroup analysis to determine for whom interventions are more or less effective. Randomized controlled trials testing how to optimize PA interventions also are needed (e.g., resistance vs aerobic training, supervised vs home based, and the optimal timing, type, intensity, and volume of PA). With the majority of cancer patients still dying from their disease, there is a need for further feasibility studies in advanced cancer patients in palliative care. In particular, there is a need for careful consideration of programming preferences, including preferences for different modes of physical activity in the design of physical activity programs to optimize recruitment, retention, and adherence. Moreover, there is a need to examine alternative forms of PA in the palliative setting, including gentler forms of PA such as yoga and Tai Chi, which may be preferable and more tolerable for individuals in the advanced stages of disease (30).
More recently, prospective observational studies have provided evidence for an association between PA and disease end points. Research suggests that for breast and colon cancer survivors, higher amounts of PA are associated with lower risks for recurrence, cancer-specific mortality, and overall mortality. There is a need for future studies to examine the relationship between postdiagnosis levels of PA in understudied groups of cancer survivors and determine the most beneficial type, intensity, frequency, and duration of PA to improve survival and prevent recurrence for each cancer group. However, observational studies cannot determine causality, and randomized controlled trials are needed. Much work remains to be done, therefore, to determine efficacious PA recommendations for each cancer group at different stages of the cancer trajectory.
Based upon the current evidence, the American Cancer Society has recommended regular exercise to cancer survivors (11). For cancer survivors undergoing adjuvant treatment, exercise is both feasible and beneficial. Low to moderate intensity exercise performed 3-5 d·wk−1 for 20-30 min is recommended, but should be tailored according to the individual's fitness level and treatment side effects. Walking is the preferred activity reported by most cancer survivors and can be performed at the recommended intensity for most cancer survivors on adjuvant therapy. Because of the accumulating side effects of most cancer treatments, exercise progression during adjuvant therapy is unpredictable; therefore, cancer survivors should be encouraged to exercise to tolerance during adjuvant therapy, including reducing intensity and performing exercise in shorter durations (e.g., 10 min) if needed. In particular, resistance exercise may be beneficial to cancer survivors during adjuvant therapy to help maintain lean body mass and prevent weight gain. Likewise, individuals in the palliative stages of the cancer trajectory are recommended to exercise to tolerance. The focus at this stage will be to maintain physical function and preserve body mass. Gentler forms of PA such as yoga and Tai Chi may be preferable and more tolerable.
During survivorship, most cancer survivors can probably be recommended the public health exercise guidelines from the American College of Sports Medicine and the U.S. Centers for Disease Control and Prevention (14). To improve or maintain general health, two different exercise prescriptions are proposed. The more traditional "vigorous" prescription is to perform at least 75 min of continuous vigorous intensity exercise (i.e., ≥75% of maximal heart rate) per week over three different days per week. The alternative "moderate" prescription is to accumulate at least 150 min of moderate intensity exercise (i.e., 50%-75% of maximal heart rate) per week over at least three different days per week in durations of at least 10 min. Combinations of vigorous and moderate intensity PA also can be performed to meet the guidelines with a simple double weighting of the vigorous minutes (e.g., 50 min of vigorous PA plus 50 min of moderate PA). To date, exercise trials in cancer survivors generally have tested the traditional prescription, and there is some evidence that QoL benefits may be enhanced if cardiovascular and strength adaptations occur. Nevertheless, in the absence of evidence to suggest the superiority of one recommendation over the other, it is likely that both prescriptions will offer similar benefits, and the more moderate intensity exercise may be more tolerable, especially during treatments. Of consideration, if weight loss is a goal, as recommended to the general population, cancer survivors may need to exercise at a greater volume. This may have particular relevance for cancers for which overweight and/or weight gain increases risk of recurrence and decreases survival (e.g., breast and endometrial cancers).
In prescribing exercise to cancer survivors, there are several factors to consider. The majority of research to date has been with breast cancer survivors who generally have a good level of functioning and a good prognosis; therefore, the evidence for these guidelines is most compelling for breast cancer survivors. The dilemma in providing specific recommendations is that each cancer survivor group is different based upon demographic, disease, and medical variables, including the different types of treatments and prognoses. To date, there are insufficient data to suggest specific recommendations for different cancer groups at different points on the cancer trajectory. Rather, similar to the general population, the general guidelines should be used as a general framework and modified to suit the needs of the individual. Further refinement of the PA prescription and widespread promotion of PA by exercise and cancer organizations promises to have a substantial impact upon the QoL of cancer survivors and, potentially, even their risk of disease recurrence and overall prognosis.
Kerry S. Courneya is supported by the Canada Research Chairs Program.
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