Despite the relatively high mortality rates for various cancers, the prospects for surviving the disease have never been better. The most recent estimate of the 5-yr relative survival rate across all cancers and all disease stages is 62% (2). This figure soars to over 90% for some of the most common cancers if they are detected early (e.g., prostate, breast, and colon). The high incidence rates and good survival rates have resulted in over 9 million cancer survivors currently alive in the United States (2). This fact has spurred a major research effort into strategies to enhance quality of life (QOL), reduce the risk of recurrence and other diseases, and extend survival in this population. The purpose of this paper is to provide an overview of the possible role of physical exercise in this effort. More specifically, I will provide a brief overview of cancer treatments and their effects on QOL, summarize the published research on exercise in cancer survivors, present recently completed trials from the University of Alberta, and offer directions for future research. Parenthetically, throughout this paper I use the term cancer survivor—as suggested by the National Coalition for Cancer Survivorship—to refer to any individual diagnosed with cancer, from the time of discovery and for the balance of life.
CANCER TREATMENTS, SURVIVAL, AND QUALITY OF LIFE
Although the outlook for surviving cancer is often very good, it almost always requires medical intervention. The most common treatment modalities for cancer are surgery, radiation therapy, and systemic therapy (i.e., drugs). These medical interventions have documented survival advantages, but the implications for QOL are not trivial. Surgery is performed on about 60% of cancer survivors. Depending on the location and extent of the operation, significant morbidity can occur (e.g., wound complications, infections, loss of function, decreased range of motion, diarrhea, dyspnea, pain, numbness, and lymphedema). Over 50% of cancer survivors may undergo radiation therapy at some point during the treatment process. Radiation therapy is typically delivered in repeated small doses (i.e., fractions) over a 5- to 8-wk period to maximize the killing of cancer cells and minimize the damage to normal cells. Nevertheless, toxicity to normal tissue does occur but is dependent on the site that is irradiated (e.g., pain, blistering, reduced elasticity, decreased range of motion, nausea, fatigue, dry mouth, diarrhea, lung fibrosis, and cardiomyopathy).
Systemic therapy (i.e., drugs) is prescribed for many cancers. The three major types of systemic therapy are chemotherapy, endocrine or hormone therapy, and biologic or immunotherapy. Chemotherapy is usually administered intravenously or orally and is given in repeated courses or cycles 2–4 wk apart over a 3- to 6-month period. Chemotherapy may cause various adverse events including fatigue, anorexia, nausea, anemia, neutropenia, thrombocytopenia, peripheral neuropathies, ataxia, and cardiotoxicity. Hormone therapy is usually administered orally (continuously or intermittently) for many years and can have significant side effects such as weight gain, muscle loss, proximal muscle weakness, fat accumulation in the trunk and face, osteoporosis, fatigue, hot flashes, and increased susceptibility to infection. Lastly, biologic therapies are the newest treatments and influence the body’s own defense mechanisms to act against cancer cells or potentiate the effects of other drugs. These treatments tend to be better tolerated but can still produce significant side effects similar to chemotherapy.
Increasingly, combinations of the main cancer treatment modalities (surgery, radiotherapy, and systemic therapy) are used to treat cancer. The timing and sequence of the treatments varies depending on the cancer and its stage. It is possible that some cancer survivors may be treated on multiple occasions with multiple modalities for many months at a time. Consequently, it is easy to see that such prolonged and intensive medical treatments may take a heavy toll on the physical, functional, emotional, spiritual, and social well-being of cancer survivors.
EXERCISE IN CANCER SURVIVORS
Research into the possible role of exercise in cancer survivors is of relatively recent vintage compared with research examining exercise and cancer prevention. The earliest study that I could locate was a 1981 unpublished master’s thesis by Linda Buettner at Bowling Green State University in Bowling Green, OH. After that, Maryl Winningham, a pioneer in the field, completed her doctoral dissertation on the topic in 1983 (68). These data were subsequently published in the mid-to-late 1980s (66,67). Sporadic publications then appeared on the topic throughout the late 1980s and early 1990s. The field did not really begin in earnest, however, until the mid-to-late 1990s when several groups in North America and Europe initiated research programs in the area. This upsurge in research led to several early (e.g., 34,41,64) and more recent (e.g., 11,19,21,22,33,49) reviews on the topic.
Given the number of recent reviews on the topic, I will only provide a summary of the literature here. The reader is directed to previous reviews for a more detailed analysis. In the present review, I have only included published articles that have isolated the effects of aerobic or resistance exercise. I divided the review into breast cancer survivors (21,41,49) and nonbreast cancer survivors (22) because the former now has a sufficient literature to warrant an independent review. I have also divided the review into two time periods—during and after treatment—because of likely differences in the prescription, motivation, safety, feasibility, and efficacy of exercise during these time periods (10). Consequently, the review is divided into four sections: (a) exercise during breast cancer treatment, (b) exercise after breast cancer treatment, (c) exercise during nonbreast cancer treatment, and (d) exercise after nonbreast cancer treatment. Finally, I review four trials that we have recently completed at the University of Alberta in Edmonton, Canada.
EXERCISE DURING BREAST CANCER TREATMENT
Fourteen studies have examined the effects of exercise during breast cancer treatment (12,23,37–39,42,43,54–58,66,67). Two of the studies used observational designs (12,23), whereas 12 tested interventions (37–39,42,43,54–58,66,67). Of the 12 intervention studies, the exercise occurred during chemotherapy in eight studies (38,39,54–57,66,67), during radiation therapy in one study (42), and during combined adjuvant therapy in three studies (37,43,58). Study designs consisted of two randomized controlled trials (RCTs) with placebo (i.e., stretching) and usual-care controls (39,66), three RCTs with usual-care controls (42,43,67), one RCT with self-directed versus supervised exercise and usual care controls (58), one pretest-posttest design with two matched controls (i.e., nonexercising cancer survivors and exercising healthy persons) (38), and five pretest-posttest designs with no controls (37,54–57). The sample sizes ranged from 10 to 99. Supervised exercise programs were reported in six of the studies (37–39,58,66,67), whereas six reported unsupervised, home-based exercise programs (42,43,54–57). Eleven studies tested an aerobic exercise intervention (four cycling (38,39,66,67), two walking (42,58), and five self-selected (43,54–57)) following traditional exercise prescription guidelines and one tested a combined aerobic and resistance training program (37). The length of the exercise programs ranged from 6 to 26 wk. The studies examined a wide range of biopsychosocial outcomes including functional capacity, body composition, mood states (e.g., anxiety and depression), symptoms (e.g., nausea, fatigue, sleep disturbances, and body dissatisfaction), and general QOL. All 12 intervention studies showed statistically significant beneficial effects of exercise during breast cancer treatment in multiple domains of functioning despite modest sample sizes. More specifically, exercise had significant beneficial effects on exercise capacity (38,39,55,56,58), body weight and composition (37,55,56,58,67), flexibility (37), fatigue (37,54,56,57), nausea (66), physical well-being (37,58), functional well-being (38), satisfaction with life (12,37), and overall QOL (12,56). Moreover, in one small observational study, self-reported exercise predicted survival (23).
Generally speaking, the studies examining exercise during breast cancer treatment were of good quality, consisting of RCT design with appropriate controls, supervised exercise sessions, an appropriate exercise stimulus, objective fitness indicators, and validated psychometric scales. The primary methodological limitations of these studies are: (a) the RCT methodology was not well described (e.g., enrollment, randomization, blinding, and analytical plan); (b) the samples were small and convenient; and (c) the exercise interventions did not coincide with the medical treatment in its entirety.
EXERCISE AFTER BREAST CANCER TREATMENT
Fourteen studies have examined exercise after breast cancer treatment (3,4,6,35,40,45,46,50,51,53,60,69). Seven of these studies used observational designs (3,6,40,45,50,51,69) and seven tested interventions (4,35,46–48,53,60). Of the seven intervention studies, two used RCTs with usual care or wait-list controls (46,60), and five used pretest-posttest designs with no controls (4,35,47,48,53). The sample sizes ranged from 12 to 28. In five studies the exercise program was supervised (4,35,46–48,53), whereas in one it was unsupervised (60). Three studies used cycle ergometer exercise (4,47,48), two studies did not specify the mode of aerobic exercise (53,60), and two studies used a combined aerobic and weight training program (35,46). Most studies followed traditional exercise prescription guidelines in terms of frequency, intensity, and duration with one study examining the effects of an acute bout of exercise (4). The most common outcomes studied were biologic (e.g., immune system, physical fitness, and lymphedema) with lesser attention paid to psychosocial variables (e.g., anxiety, depression, and satisfaction with life). In terms of results, almost all studies showed some improvements after the exercise program including benefits to exercise capacity (46), number of monocytes (48), natural killer cell cytotoxic activity (47), depression (60), anxiety (4,60), mood (50), self-esteem (3,45), physical well-being (51), satisfaction with life (47), and overall QOL (69).
Compared with the studies on exercise during breast cancer treatment, the studies on exercise after breast cancer treatment were generally less methodologically rigorous. Only two of the 14 studies had controls (46,60), and eight of the studies relied on self-reports of exercise (3,6,40,45,50,51,60,69). Other limitations of the intervention studies include small convenience samples, relatively short exercise interventions, heterogeneous participants that spanned the survivor continuum from several months to many years postdiagnosis, and limited follow-up. Finally, the observational studies were all cross-sectional with one exception (51).
EXERCISE DURING NONBREAST CANCER TREATMENTS
Ten studies have examined the effects of exercise during treatments for cancers other than breast (14,17,24–29,44,63). Four of the studies examined mixed cancer survivors (e.g., breast, testicular, non-Hodgkin’s lymphoma, and multiple myeloma) immediately after high-dose chemotherapy and bone marrow/peripheral blood stem cell transplantation (26–29); two studies examined leukemia survivors immediately after high-dose chemotherapy and bone marrow transplantation (24,25); and one study each examined adolescents with mixed cancers (e.g., leukemia) on mixed chemotherapies (63), adults with mixed cancers (e.g., Hodgkin’s and non-Hodgkin’s lymphoma) on mixed treatments (17), postsurgical stomach cancer survivors (44), and postsurgical colorectal cancer survivors (14). Three of the studies used observational designs (14,17,28), and seven tested interventions (24–29,44,63).
Of the seven intervention studies, five used an RCT design with usual-care controls (24,26,29,44,63), and two used a pretest-posttest design with no controls (25,27). The sample sizes ranged from 5 to 70. Supervised exercise programs were reported in six studies (24,26,27,29,44,63), whereas one reported a home-based exercise program (25). Using traditional exercise prescription guidelines, six of the studies tested an aerobic exercise intervention (three cycling, two walking, and one mixed aerobic exercise) (25–27,29,44,63), whereas one intervention focused on resistance exercise (24). The length of the exercise programs ranged from 2 to 16 wk. The studies examined a wide range of biopsychosocial outcomes including functional capacity, body composition, natural killer cell cytotoxic activity, mood states (e.g., anxiety and depression), symptoms (e.g., nausea, fatigue, pain), and general QOL. All seven intervention studies showed significant beneficial effects of exercise during cancer treatment in multiple domains of functioning despite some small sample sizes. The reported outcomes included improvements in exercise capacity (26,27,63), body composition (63), natural killer cell cytotoxic activity (44), neutropenia (26), thrombocytopenia (26), diarrhea (26), pain (26), required platelet transfusions (26), length of hospitalization (17,26), anxiety (17,28,29,63), depression (17,28,29), vigor (28), anger (29), fatigue/energy (17,27), physical well-being (14,17), functional well-being (14,17), emotional well-being (14), social well-being (14), and satisfaction with life (14).
Overall, similar to studies on exercise during breast cancer treatment, the studies on exercise during nonbreast cancer treatment were generally of good quality consisting of RCT designs with appropriate controls, supervised exercise sessions, an appropriate exercise stimulus, objective fitness indicators, and validated psychometric scales. Once again, however, the primary methodological limitations of these studies are: (a) the RCT methodology was not well described, (b) the samples were small and not representative, and (c) the exercise interventions did not coincide with the medical treatment in its entirety.
EXERCISE AFTER NONBREAST CANCER TREATMENTS
Nine studies have examined exercise after treatments for cancers other than breast (13,30–32,36,40,52,61,62). Four studies examined mixed cancer survivors (e.g., breast, non-Hodgkin’s lymphoma, leukemia, and prostate) (30–32,52); two studies examined mixed childhood/adolescent cancer survivors (e.g., Hodgkin’s, lymphoma, leukemia) (36,62); and one study each examined prostate cancer survivors (40), head/neck cancer survivors (61), and colorectal cancer survivors (13). Three of these studies used observational designs (13,36,40), and six tested interventions (30–32,52,61,62). Of the six intervention studies, two used pretest-posttests with matched controls (30,61), and four used pretest-posttests with no controls (31,32,52,62). The sample sizes ranged from 6 to 32. Most studies reported supervised exercise interventions (30–32,61,62) with one using home-based exercise (52). One study used a walking program (30), four studies used a mixed aerobic and resistance program (31,32,52,61), and one study used an unspecified aerobic program (62). Four of the six studies followed traditional exercise prescription guidelines in terms of frequency, intensity, and duration (30–32,62). The studies examined biopsychosocial outcomes including functional capacity, body composition, hemoglobin levels, and general QOL. In terms of results, exercise resulted in improvements in exercise capacity (30–32,62), muscular strength (31,32), hemoglobin concentration (30), fatigue (30), depression (36,52), anxiety (52), physical appearance (36), and overall QOL (13,31,32,52).
As a group, the studies on exercise after treatments for nonbreast cancer were not as methodologically rigorous as the studies during treatment. No studies were RCTs with appropriate controls. The samples were small and heterogeneous.
RECENTLY COMPLETED EXERCISE TRIALS AT THE UNIVERSITY OF ALBERTA
We have recently completed four outcome trials at the University of Alberta in Edmonton, Canada. In this next section, I briefly describe the purpose of each trial, the exercise intervention we tested, the main outcomes and measures, and the published results to date. The trials are presented in the order in which they were initiated.
The Colorectal Cancer and Home-Based Physical Exercise (CAN-HOPE) trial.
Our first trial, the CAN-HOPE trial, was an RCT designed to examine the effects of a home-based exercise program on QOL and physical fitness in postsurgical colorectal cancer survivors (15). About 55% of participants were receiving adjuvant therapy at the time of the exercise intervention. We randomly assigned 102 colorectal cancer survivors in a 2:1 ratio to an exercise (N = 69) or control (N = 33) group. The exercise group was asked to exercise on their own 3–5× wk−1 for 16 wk at a moderate intensity for at least 20–30 min each time. The control group was asked not to begin a structured exercise program. Outcomes were assessed at baseline and postintervention. Physical fitness was assessed by a submaximal treadmill test, a sit-and-reach-test, and a skinfold test. QOL was assessed by the Functional Assessment of Cancer Therapy-Colorectal (FACT-C) scale (65).
We had 91% of participants complete the trial and a 76% adherence rate in the exercise group. Unfortunately, we also had 52% of the control group report regular exercise. Not surprisingly, we did not find any intention-to-treat effects in the outcomes paper (15). In an “on treatment” ancillary analysis, however, we found that participants who increased their fitness over the course of the intervention had more favorable changes in anxiety, depression, overall QOL, and satisfaction with life than participants who decreased their fitness over the course of the intervention. The CAN-HOPE trial was the first to test an exercise intervention in colorectal cancer survivors, and notwithstanding the major exercise adherence and contamination problems, the findings suggest that improving fitness in this group of survivors may be associated with improvements in psychosocial functioning and overall QOL. More rigorous RCTs are needed to definitively answer this question.
The Group Psychotherapy and Home-Based Physical Exercise (GROUP-HOPE) trial.
The GROUP-HOPE trial was an RCT designed to determine whether a home-based exercise program could improve QOL in cancer survivors beyond the known benefits of group psychotherapy (16,20). About 44% of the participants were receiving adjuvant therapy at the time of the intervention. We randomly assigned 22 group psychotherapy classes consisting of 108 cancer survivors to group psychotherapy alone (11 classes; N = 48) or group psychotherapy plus exercise (11 classes; N = 60). The exercise group was asked to exercise on their own 3–5× wk−1 for 10 wk (the length of the classes) at a moderate intensity for at least 20–30 min each time. The control group was asked not to begin a structured exercise program. Outcomes were assessed at baseline and postintervention. Physical fitness was assessed by a submaximal treadmill test, a sit-and-reach-test, and a skinfold test. QOL was assessed by the Functional Assessment of Cancer Therapy-General (FACT-G) scale (7).
We had 89% of participants complete the trial and an 84% adherence rate in the exercise group. We also had a more modest 22% of the control group report regular exercise. In the outcomes paper from this trial (20), we found significant intention-to-treat effects in favor of the exercise group for functional well-being, fatigue, and sum of skinfolds. We also found borderline significant effects (P < 0.10) for physical well-being, satisfaction with life, and flexibility. This trial was the first to compare exercise with another validated QOL intervention in cancer survivors, and despite some minor problems with exercise adherence and contamination, the results showed that exercise may be a useful adjunct to group psychotherapy for enhancing QOL, especially physical and functional well-being.
In the determinants paper from the GROUP-HOPE trial (16), we examined the correlates off exercise adherence (i.e., exercise in the exercise group) and contamination (i.e., exercise in the control group). We used the theory of planned behavior (1) and the five-factor model of personality (8). Interestingly, the independent correlates of exercise adherence and contamination were different in kind as well as degree. More specifically, exercise adherence was predicted by sex (male), extraversion, normative beliefs (negative), and perceived behavioral control, whereas exercise contamination was predicted by past exercise, sex (male), and intention. This information may be useful in designing RCTs that will maximize exercise adherence and minimize exercise contamination in this population.
The Resistance Exercise and Prostate Cancer trial.
The Resistance Exercise and Prostate Cancer trial was an RCT designed to determine the effects of supervised resistance exercise training on muscular fitness and QOL in prostate cancer survivors being treated with androgen deprivation therapy. It was a dual-center trial headed by the Ottawa Regional Cancer Center in Ottawa, Canada. Participants (N = 155) were randomly assigned to an exercise (N = 82) or control (N = 73) group. The exercise group performed nine resistance exercises 3× wk−1 at 60–70% of one repetition maximum for a 12-wk period. The control group did not train. Outcomes were assessed at baseline and postintervention. The primary outcomes were fatigue and QOL—as assessed by the FACT measurement system (7)—and the secondary outcomes were upper-body and lower-body muscular fitness—as assessed by standard load tests for the chest press and leg press.
We had 87% of participants complete the trial and a 79% adherence rate among the exercise group. The control group did not exercise. In the main outcomes paper (59), we found statistically significant differences in change scores favoring the exercise group for fatigue, QOL, and upper-body and lower-body muscular fitness. Moreover, we found that these differences held for men who were being treated with palliative versus curative intent and for men who had been treated for shorter than versus longer than 1 yr.
The Rehabilitation Exercise for Health after Breast Cancer (REHAB) trial.
The REHAB trial was an RCT designed to determine the effects of supervised aerobic exercise training on cardiopulmonary, QOL, and biologic outcomes in postmenopausal breast cancer survivors who had completed surgery, radiotherapy, and/or chemotherapy. About half of the participants were on hormone therapy (tamoxifen) at the time of the intervention. We randomly assigned 53 breast cancer survivors to an exercise (N = 25) or control (N = 28) group. The exercise group trained on cycle ergometers 3× wk−1 at a moderate intensity progressing from 15 to 35 min over a 15-wk period. The control group did not train. Outcomes were assessed at baseline and postintervention. The primary outcomes were peak oxygen consumption—as assessed by a graded exercise test using gas exchange analysis—and overall QOL—as assessed by the Functional Assessment of Cancer Therapy-Breast (FACT-B) scale (5).
We had 98% of participants complete the trial and a 98% adherence rate among the exercise group. The control group did not exercise. In the cardiopulmonary and QOL outcomes paper (18), we found statistically significant differences in change scores favoring the exercise group for peak oxygen consumption, peak power output, overall QOL, happiness, fatigue, and self-esteem. Moreover, we also found that some of the changes in QOL were mediated by changes in cardiopulmonary function. The biologic outcomes will be analyzed in separate papers.
CONCLUSIONS AND FUTURE DIRECTIONS
There is a growing interest in the possible role of exercise in enhancing QOL, reducing recurrence and other diseases, and extending survival in cancer survivors. Preliminary research suggests that exercise may be an effective intervention for enhancing QOL in cancer survivors and that this effect may be beyond that provided by group psychotherapy. The studies are few in number, however, and of limited quality. Future research using rigorous RCT methodology is needed to definitively answer questions concerning the role of exercise in enhancing QOL in cancer survivors both during and after treatment. Moreover, research should be extended beyond breast cancer survivors to the many other cancer groups who may benefit from exercise. For breast cancer survivors, there is sufficient evidence to warrant second generation studies focusing on more specific questions such as the optimal timing, type, frequency, intensity, duration, progression, and context for exercise (9). Studies are also needed to examine mechanisms of change for QOL and to compare and integrate exercise with other currently accepted QOL interventions (9).
It is unknown whether exercise will reduce the risk of recurrence, other diseases, or extend survival after a cancer diagnosis. Future research is needed to examine the effects of exercise on promising biomarkers of disease and, ultimately, cancer recurrence and overall survival. Taken together, the promising findings to date suggest that exercise scientists may play an important role in cancer control efforts at the clinical and population levels.
Kerry S. Courneya, Ph.D., 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 with funds from the Canadian Cancer Society and the Sociobehavioral Cancer Research Network. I would like to acknowledge the many colleagues, graduate students, and research participants who have contributed to this research.
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