Background
Cancer has been the number one cause of death since 1983 and poses a major public health concern in Korea [
1]. The incidence rate of all cancers showed an annual increase of 3.3% between 1999 and 2009 [
1]. There were 192,561 cancer cases and 69,780 cancer deaths in 2009 in Korea [
1]. The cumulative risk of developing cancer during a lifetime was 37.9% for men and 32.7% for women [
1]. Despite notable improvement in five-year relative survival rates for all cancers in Korea [
2], a large number of cancer patients still experience cancer recurrence. Therefore, identifying the factors that contribute to cancer recurrence and survival is important.
Beneficial effects of exercise and physical activity on health-related fitness, quality of life, and other patient-reported outcomes among cancer survivors during and after treatment have been reported previously [
3-
11]. A recent meta-analysis reported that physical activity is associated with reduced all-cause, breast cancer–specific, and colon cancer–specific mortality [
12,
13]. In addition to the benefits of physical activity on the health of cancer survivors, the American College of Sports Medicine (ACSM) reported that participation in exercise and physical activity is safe during and after adjuvant cancer therapy [
14].
Despite these and other well documented benefits of exercise and physical activity and the safety of participating in exercise, many cancer patients still remain physically inactive [
15]. Only 29.6% of cancer survivors met the exercise recommendations of the ASCM [
16], significantly less than the percentage among the non-cancer population. Another meta-analysis also reported that 53–72% of cancer survivors do not meet ACSM exercise guidelines for cancer patients [
17]. Although we have recently identified that there were no significant difference in total physical activity time between pre-diagnosis and on-treatment among colorectal cancer patient [
18], participation in exercise declines substantially during cancer treatment and may not return to pre-diagnosis levels of exercise after treatment is completed [
15]. Therefore, it is important to find strategies to increase exercise participation in cancer patients.
Jones et al. [
17] reported that simple oncologist’s physical activity recommendation increased their patient’s physical activity levels in women newly diagnosed with breast cancer. Another study found that a physician’s recommendation regarding physical activity has been demonstrated to be a strong predictor of a patient’s level of physical activity [
19,
20]. Nevertheless, although cancer patients are highly motivated to receive exercise information from their oncologists [
19,
20] and oncologists have a favorable view on exercise for their patients, most oncologists still do not recommend exercise for their patients [
16,
17,
21,
22]. However, barriers to oncologists’ recommendation of exercise to their patients have not been studied fully. Furthermore, the oncologists’ attitude toward recommending exercise and practice of exercise recommendations to their cancer patients has not been studied. Furthermore, whether factors such as their attitudes toward exercise and their own physical activity levels may influence oncologists’ recommendations toward exercise and the barriers they experience in recommending exercise have not been studied.
The purposes of this study were to evaluate 1) the attitudes of oncologists toward recommending exercise, 2) the association between oncologists’ own physical activity levels and the attitudes of oncologists toward recommending exercise, and 3) the barriers experienced by oncologists in recommending exercise to their patients.
Discussion
Previous studies demonstrated that cancer patients tend to exercise more if they receive exercise recommendations from their oncologists [
16,
17,
21,
22]. In the present study, we have identified the characteristics of exercise recommendations among oncologists, the characteristics of exercise recommendations based on oncologists’ own physical activity levels, the perceived benefits of exercise among oncologists, and the barriers oncologists perceive to recommending exercise to their patients. Most oncologists believe that exercise during treatment is beneficial and important for cancer patients. However, fewer oncologists agreed that exercise during treatment is safe or easy. Furthermore, most oncologists thought very positively about recommending exercise to their patients during treatment. Only a small number of oncologists thought negatively about recommending exercise to their cancer patients. However, just 7.2% of oncologists agree that their cancer patients manage to exercise during cancer treatment. Therefore, our findings show, first, that most oncologists think that exercise during cancer treatment is beneficial and important but that they have concerns about the safety of exercise, and, second, oncologists thought that very few of their patients are actually exercising during cancer treatment in Korea.
Unlike the opinions of the oncologists in the current study that only 7.2% of cancer patients manage to exercise during cancer treatment, a previous study showed that 37% of colorectal cancer survivors and 28% of breast cancer survivors participate in regular physical activity during treatment [
18,
28]. Furthermore, 32% of breast cancer survivors actually participated in recommended levels of physical activity, defined as 150 min per week of moderate to vigorous intensity sports/recreational physical activity, after the completion of treatment [
15]. Blanchard and colleagues examined the prevalence of physical activity in 9105 cancer survivors [
29] and reported that 30–47% of survivors of cancer are meeting the physical activity recommendations. In Korean cancer patients, we have recently determined that 7.6% of Korean colorectal cancer patients participated in more than ACSM guidelines (150 min per week of moderate to vigorous physical activity) during cancer treatment, significantly lower patients than the 20.5% who participated physical activity more than ACSM guideline during before the cancer diagnosis [
18]. However, the reason why the percentage of individuals meeting ACSM guidelines decreased during treatment is due to reduced vigorous intensity of physical activity, while the amount of mild intensity physical activity tended to increase during treatment (111.1 ± 203.9 min versus 146.8 ± 232.2 min) compared to before cancer diagnosis [
18]. Although there is a possibility of over reporting of the level of physical activity among cancer survivors [
30], the results of the current study may suggest that oncologists in Korea may underestimate the exercise ability of their cancer patients.
The attitudes of oncologists toward exercise and toward recommending exercise are very important since the exercise recommendations of oncologists are a strong predictor of cancer patients’ participation in exercise [
31]. Previous studies indicated that cancer patients are highly motivated to receive advice on exercise and that they consider their oncologist an important source of this information [
17,
19]. Jones and colleagues [
19] surveyed 311 survivors of prostate, breast, colorectal, or lung cancer, and a total of 84% of the participants indicated that they would prefer to receive exercise counseling during their cancer experience. Our study showed that over 70% of oncologists believed that exercise is important and beneficial to cancer patients. Our study further showed that 87% of oncologists believed that providing exercise recommendations to cancer patients is not hard, but only 40% of oncologists actually recommended exercise to their patients in the past one month. These results are similar to those of previous studies, which found that approximately 43% and 44% of oncologists regularly provided exercise recommendations and/or discussed exercise with their patients when appropriate [
16,
21].
To understand whether individual physical activity participation levels influence exercise recommendations and attitudes toward exercise recommendations, we also examined the oncologists’ own physical activity levels. Our analysis showed that only 11.9% of the surveyed oncologists met ACSM physical activity guidelines, a rate notably lower than that for oncologists of several other countries, such as the 52.5% of Canadian oncologists [
21] or 57.3% of American oncologists [
25] who met the guidelines. Our analysis also showed that the oncologists’ own physical activity participation was associated with their attitude toward exercise recommendation to their patients. Those who participated in more physical activity believe that their patients think that they should recommend exercise; they also think that recommending exercise is dependent on them and they tried to recommend exercise to their patients more.
In our study, we also surveyed the oncologists’ perceived benefits of exercise for cancer survivors. They believed that exercise participation would improve the ability of patients to perform daily tasks (26.7%), improve mental health (24.6%), attenuate physical decline from treatment (19.2%), reduce body weight (9.2%), and reduce the risk of other diseases (7.7%). It is interesting that only 4.8% of oncologists actually think that exercise may reduce cancer recurrence, while many reported studies have shown that exercise reduced the recurrence of various cancers [
12,
13].
A growing number of large observational studies have reported that physical activity reduces all-cause and cancer-specific mortality, which suggests that exercise may confer additional improvements in breast and colorectal cancer survival beyond surgery [
32-
34]. Holmes et al. [
32] demonstrated that women with breast cancer who participated in more than 9 metabolic equivalent (MET) hours per week of physical activity have a 41%, 50%, and 43% reduction in the risk of total death, breast cancer death, and risk of recurrence, respectively, compared with those who participated in fewer than 3 MET hours per week of physical activity. Meyerhardt et al. [
35] also demonstrated that more than 18 MET hours per week of physical activity after diagnosis is associated with a 45-61% reduction in the risk of colorectal cancer-specific death and a 57-63% reduction in the risk of total death. Although it is beyond the scope of our study, it may be interesting to ascertain whether knowledge of the impact of physical activity on cancer recurrence and mortality would influence the oncologists’ patterns of physical activity and exercise recommendations. In our study, we analyzed whether oncologists’ perceived benefits of exercise for cancer patients would be associated with their exercise recommendations. We observed that oncologists who believe that exercise will improve patients’ mental health as well as reduce the risk of other diseases recommended exercise to their patients significantly more than those who do not think exercise will have such benefits for their patients. Based on these results, we can speculate that knowledge of the impact of exercise on cancer patients may also influence the patterns and characteristics of exercise recommendations. The result of our study may suggest that the information on the validated benefit of exercise for cancer survivors should be easily available for oncologists to increase their exercise recommendation to patients more. Since cancer survivors’ exercise/physical activity behavior is easily influenced by oncologists’ exercise and physical activity recommendation, difference in exercise recommendation percentage of oncologists may actually have clinical relevance.
In assessing the factors which make it difficult to recommend exercise, lack of time during office visits, unclear recommendations, and concerns about the safety of exercise were the three most prevalent answers. Herbert et al. [
36] reported that the most common barriers to providing physical activity counseling by primary care provider’ to patients in a clinical setting were lack of time, lack of knowledge, and lack of success in changing patient behavior. Not having sufficient time during office visits is a significant barrier to recommending exercise for many oncologists, since doctors spend, on average, less than 5 minutes during an office visit [
37]. However, knowing that oncologists’ 30-second exercise recommendation increased patients’ physical activity level by 3.4 MET hours per week in breast cancer patients [
17], it would be important to develop and provide an exercise recommendation tool to assist oncologists in providing effective exercise recommendations in a short time. Unclear recommendations and concerns about safety, meaning unclear guidelines for cancer patients, are also significant barriers for oncologists in recommending exercise to their patients. The ACSM Roundtable on Exercise Guidelines for Cancer Survivors [
14] concluded that exercise training is safe during and after cancer treatments and results in improvements in physical functioning, quality of life, and cancer-related fatigue in several cancer survivor groups. In addition, other studies in cancer types including breast cancer, colorectal cancer, and prostate cancer have continually shown that exercise for cancer patients during and after treatment is safe [
14]. In our analysis, we found that oncologists who were unclear about exercise recommendations and who had concerns about the safety of exercise recommended exercise to their patients significantly less. Therefore, it is important to provide information on the safety of exercise in cancer patients to oncologists.
Although the present study provides important information regarding oncologists’ attitudes toward exercise, there are several limitations that need to be considered when interpreting the results of this study. A selection bias is likely to exist because of the transparent purpose of the study, and the relatively low response rate to our survey may limit the generalizability of our findings. Furthermore, a possible response bias is another limitation; oncologists who were more interested in physical activity were probably more likely to respond. Another important limitation is the use of a retrospective observational design that provides the weakest evidence in terms of causality and is susceptible to memory biases. As such, it is possible that oncologists may have recalled numerous discussions with patients interested in exercise and not those with all patients, which therefore would overestimate the actual recommendation rates. Future research is required using prospective designs with objective measures of a patient–oncologist discussion of exercise (e.g., audiotaped consultation review). Lastly, since the current study is a cross-sectional study, it is not possible to identify the cause and effect relationship between variables.
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Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
JH, as first author of this paper, she made the idea of this research initially, designed it, organized all process of research, analyzed and wrote the manuscript. MS collected all of data, and wrote the manuscript. YJ and CW planned the research design, and involved in all of the process. LW involved in a planning of the research design, and wrote the manuscript. SI and NK involved in a planning of the research design, organized all progress of data collecting, and wrote a manuscript. J.Y., as corresponding author of this paper, he initially designed the study, and supervised all the progress of this research. He also dealt whole manuscript writing. All authors read and approved the final manuscript.