Colorectal cancer is the cause of 13% of cancer deaths (13). The survival rate 5 yr after diagnosis can reach up to 90.3% when the tumor is detected at the initial stages (16). However, recurrence rates can reach up to 60% (22). A recent study concluded that colon cancer in some subgroups results in a similar survival rate to that of people without cancer, which highlights the importance of cancer nonrecurrence (27). Physical activity and body composition play vital roles in the prevention of cancer recurrence (23). Therefore, health support programs to control or improve these risk factors are needed.
Colon cancer survivors (CCS) suffer from a reduction in health-related fitness, both objectively and perceptively (31), including decreases in balance, flexibility, functional capacity, and the isometric strength of abdominal muscles. This decrease not only affects the patient’s functional ability but is also accompanied by a decrease in abdominal muscle width (32), which could lead to the development of chronic low back pain. Therefore, an effective choice of intervention for these patients should consider the rehabilitation of the lumbopelvic area. However, we are not aware of previous studies that describe a specific protocol for training this area of the body in CCS.
Reduced isometric strength of the abdominal wall muscles in colon cancer patients who underwent longitudinal abdominal incisions has been demonstrated (11). This reduction in isometric strength in abdominal flexor muscle can reach up to 65% compared with the strength of healthy controls (31). CCS also show a decrease in fatigue resistance in the soleus, a postural muscle in the legs (28). Evidence indicates that a therapeutic approach to prevent this loss should be directed at the stimulation of mitochondrial biogenesis and the reduction of muscle proteolysis and inflammation (1). Physical activity reduces the loss of muscle mass and improves mitochondrial content (4). Therefore, a muscle stabilization exercise program could improve motor control in lower back and pelvic muscles. A physical activity program based on muscle stabilization exercises, such as Pilates-based exercise programs, may be an option to solve this problem. However, no studies have demonstrated the effects of this type of exercise program in CCS.
Currently, gaining popularity, muscle stabilization programs promote improvements in the strength and control of trunk muscles, endurance, flexibility, balance, and breathing (17). Indeed, the beneficial effects of these programs have been widely studied because these programs have positive effects on quality of life (5,7), physical fitness, mood (5), postural balance (7), fall prevention (5), and body composition (29) in older people. However, few studies have used muscle stabilization exercises in cancer patients.
The American College of Sports Medicine expressed the need in 2010 for increased research to expand our knowledge of the safety and efficacy of Pilates in treating cancer patients (34), in which motor control of the lumbopelvic area is addressed based on a specific training philosophy. In addition, it has been shown that the Pilates program gives similar results for improving muscle endurance to those of traditional resistance programs in breast cancer patients (20) and that it increases functional capacity and flexibility (12), shoulder functionality, quality of life, mood, and body image (38) in patients with this type of cancer. However, it is necessary to enhance the effects of stabilization exercise programs based on Pilates in cancer patients, especially in colon cancer patients.
The present study evaluated the effects of a physical activity program incorporating lumbar and pelvic stabilization exercises on health-related fitness, anthropometric measurements, and body composition in CCS. We hypothesized that a CO-CUIDATE exercise program based on lumbopelvic exercises would improve health-related fitness, anthropometric measurements, and body composition end points compared with the effects of the usual-care protocols.
For this randomized controlled clinical trial, 46 CCS (35% female, n = 14) were assigned to one of two groups within 1 yr of their completion of primary treatment (Clinical Trials.gov NCT02052050): a group undergoing a trunk muscle stabilization exercise program (CO-CUIDATE group) and a usual-care group. The study was performed from September 2013 to December 2014. Participants were recruited from the Department of Surgery at the University Hospital San Cecilio, Granada (Spain), and they were eligible if they 1) were more than 18 yr old, 2) received curative treatment due to cancer (surgery, chemotherapy, and/or radiotherapy), 3) were diagnosed with grades I to IIIA of colorectal cancer, and 4) completed coadjuvant treatment. Subjects were excluded if they presented cancer recurrence, underwent previous abdominal surgeries, or diagnosed with concomitant conditions, such as previous lower-back pain or musculoskeletal conditions (e.g., osteoarthritis, fibromyalgia, or chronic fatigue syndrome).
Two oncology surgeons at the hospital encouraged patients to participate in the study to stimulate subject participation (24). Interested participants were called and fully informed about the study. An appointment was scheduled, and after passing a medical and physical examination, patients signed a consent form. The Research Ethics Committee (Granada, Spain) granted ethical approval (CEI2013-MP-18) for the study, and the trial followed the Helsinki Declaration for biomedical research (14/2007).
Epidat 3.1 software (Xunta de Galicia, Spain) was used to calculate the sample size. The sample size was based on detecting a minimum difference of 29.19 s in the posttreatment abdominal isometric endurance scores, according to previous research using a similar exercise program in breast cancer survivors (8), with an α level of 0.05, a desired power of 80%, and an estimated standard deviation of ±29 s. Each group included 18 participants. We chose 23 participants for each group assuming a 20% dropout rate.
Participants were placed into two groups (CO-CUIDATE or control group) in two randomized cycles (block size = 23) using computer-generated numbers from Epidat 3.1 software (Xunta de Galicia, Spain), and the sequence created was introduced in numbered, opaque, sealed envelopes by an external researcher who did not participate in the study. The envelopes were opened to obtain group assignments after the participants were evaluated.
Two physiotherapy experts in oncological rehabilitation with more than 7 yr of experience working with oncology patients performed the CO-CUIDATE program, which was conducted in 90-min sessions three times per week for 8 wk. Each session included warm-up exercises (10–20 min), core stabilization exercises (20–30 min), and stretching exercises (Table 1). The exercises were adapted to each participant’s potential. Each patient kept a diary throughout the exercise program to register perceptions of fatigue (Borg RPE scale) and adverse effects of the program. Adherence was defined based on the patient’s attendance of the CO-CUIDATE sessions, and patients were considered as dropouts if they did not participate in at least 18 (75%) of 24 sessions.
The control group received the usual treatment, which was stipulated by their oncologist. It consisted of some general recommendations for a healthy lifestyle that were delivered at the start of the program in paper format. Their physical activity level was controlled for during the study period to avoid a possible bias through a follow-up assessment using the Spanish version of the Minnesota Leisure questionnaire. Control subjects were assessed at the same times as the CO-CUIDATE group (baseline, 8 wk, and 6 months). For ethical reasons, control patients were allowed to participate in the same exercise program as the CUIDATE group once the study period was completed, but these data were excluded from the analyses.
End Points and Measurements
Health-related fitness end points
The primary outcome was isometric abdominal strength, which was assessed using the trunk curl test. Patients remained in a supine position with a 90° flexion of both knees and hips and with their arms extended without touching their knees. Patients performed a trunk curl and maintained an isometric position that separated the inferior angle of the scapulae from the stretcher for as long as possible up to a maximum of 90 s (21). This test exhibits an intraclass correlation coefficient (ICC) > 0.97 (22).
Secondary end points
Physical end points
Isometric back strength was measured using a back dynamometer (TKK 5002 Back-A; Takey, Tokyo, Japan) with a precision of 1 kg. Patients were measured in a standing position with a lumbar flexion of 30°, and they performed an extension of the trunk three times. The average value was used for analyses. This test showed acceptable to good reliability (ICC = 0.81 and 0.85) (14).
Functional capacity was determined based on a walking test used to measure the distance (m) that patients could walk in 6 min. This test was performed using a treadmill (H-P-COSMOS for graphics; Germany) after previous training, and patients were allowed to increase or decrease the treadmill speed. This test is reliable in cancer patients (ICC > 0.93) (33).
Lower-body flexibility was assessed using a chair sit-and-reach test. Patients were instructed to slide their hands forward as far as possible to touch their toes. The distance between the tip of the fingertips and the toes was measured. If the fingertips touched the toes, the score was zero. If the fingertips did not touch the toes, the distance between the fingers and the toes was measured as a negative score. If the fingers overlapped the toes, the distance of the overlap was measured as a positive score. Two trials with each leg were performed, and the average of both legs was included in the analysis (31). The reliability of this test exhibited an ICC = 0.94 (9).
These physical tests have been used previously with colon cancer patients (31), and all of these tests were conducted with multiple observations.
Anthropometric end points
Waist and hip circumferences were measured using a plastic tape measure. Waist circumference was assessed midway between the lower rib margin and the top of the iliac crest (cm) at the end of a normal breath. Hip circumference was measured at the level of the greater trochanter. The ICC values for waist and hip circumferences were 0.89 and 0.81, respectively (37).
Height and body composition was assessed using bioelectrical impedance (InBody 720; Biospace, Gateshead, UK). Height, body fat percentage, skeletal muscle mass (kg), and body mass indexes were recorded for analysis. The instrument used exhibits high reliability (39).
A trained member of the research group with 5 yr of experience in taking these measurements on cancer patients and who was blinded to patient group assessed these variables at the three time points. Measurements were performed in the physiotherapy laboratory of the Faculty of Health Sciences at the University of Granada (Spain).
Mean, 95% confidence interval (CI), and standard deviation were used in descriptive analyses. Student’s t-test and chi-square test were used to assess the ability of the randomization process to avoid differences between groups at baseline. The Shapiro–Wilk test was used to assess the normality of the distribution of the variables.
A repeated-measure ANCOVA between the three time points (baseline, postprogram, and 6 months of follow-up) was used to examine the between-group and within-subject differences. Patient age and tobacco and alcohol use were used as covariates to examine the influence of these variables on the main analysis of this study. Cohen’s d was calculated to examine intergroup effects and to determine whether there were small (d < 0.2), negligible (0.2 < d > 0.5), moderate (0.5 < d > 0.8), or large (d > 0.8) differences (10).
The Statistical Program for Social Sciences (IBM, SPSS version 22.0) was used for statistical analyses with a 1% level of significance for all statistical tests, and analyses were performed according to the intention-to-treat principle. The worst-case value was used to replace missing data, after a previously reported procedure (30).
Seventy-seven CCS were evaluated with regard to the inclusion criteria. The 46 patients who met the criteria were randomized into two groups: 23 patients in the CO-CUIDATE group and 23 patients in the usual-care group. Figure 1 illustrates the number of CCS randomized into each group; the number of and reasons for dropouts are also shown. There were two dropouts (10.5%) in the CO-CUIDATE group (reasons: never started the program, n = 1; too busy, n = 1) and four dropouts (17.4%) in usual-care group (reasons: health problems, n = 1; family problems, n = 1; too busy, n = 2). Table 2 shows the demographic, clinical, and medical characteristics of the sample group. There were no significant differences between groups for any variable at baseline (Table 3). Adherence rates were calculated as the ratio of the number of exercise sessions performed relative to the number of sessions prescribed. The average attendance of the CO-CUIDATE group was 22.0 ± 1.1 of the 24 sessions, with an adherence rate of 88.36%. Two participants in the CO-CUIDATE group and one participant in the usual-care group experienced postoperative ventral hernias. In the first sessions of the program, six patients expressed both neck and abdominal discomfort with some of the exercises (roll up–roll down and saw). They subsequently underwent a slower progression and received more support to achieve the goals of the program. Furthermore, one patient could not perform the aerobic exercise during 1 wk because he suffered a peripheral neuropathy. The average range of the perception of fatigue was 12 (6–17).
Health-related fitness end points
ANOVA revealed a significant difference (F = 7.7, P = 0.001) in the group–time interaction for isometric abdominal strength. The CO-CUIDATE group experienced a greater increase in isometric abdominal strength compared with that of the usual-care group after discharge (Table 4). The intergroup effect size was large after the 8-wk program (d = 1.2, 95% CI = −4.9 to 7.5). The covariates did not influence these results. Analysis of isometric back strength (F = 2.1, P = 0.13) revealed a nonsignificant trend for the group–time interactions, with a greater increase in the CO-CUIDATE group compared with that in the usual-care group (Table 4).
Physical end point analyses
Statistical analyses revealed significant differences in group–time interactions for the remaining physical variables: functional capacity (F = 4.6, P = 0.015) and right and left lower-body flexibility (F = 4.3, P = 0.021 and F = 3.6, P = 0.034, respectively). The CO-CUIDATE group exhibited a higher increase in functional capacity and lower-body flexibility compared with the results in the usual-care group after discharge (Table 4). Intergroup effect sizes observed after the exercise program were large for functional capacity (d = −0.8, 95% CI = −27.7 to −26.0) and for right and left lower-body flexibility (d = −0.8, 95% CI = −2.7 to 1.0 and d = −0.8, 95% CI = −3.5 to 1.7, respectively). Effect sizes at the 6-month follow-up were large for functional capacity (d = −0.9, 95% CI = −27.5 to 29.3). The inclusion of age as a co-variable in the analysis influenced right (F = 2.8, P = 0.068) and left lower-body flexibility (F = 2.1, P = 0.135).
Anthropometric end point analyses
A significant group–time interaction was found for waist circumference (F = 5.5, P = 0.007). The CO-CUIDATE group experienced a greater decrease in this variable compared with results in the usual-care group (Table 5). Intergroup effect sizes for waist circumference were large after the exercise program (d = 0.9, 95% CI = −0.7 to 2.6) and moderate at the 6-month follow-up (d = 0.7, 95% CI = −0.3 to −1.7) (Table 5). The inclusion of additional covariates did not significantly change these results. There were no significant differences in the group–time interactions for the variables of hip circumference, weight, or body composition.
The results of this randomized trial partially confirm our hypothesis that the CO-CUIDATE program widely improves isometric abdominal strength, functional capacity, and lower-body flexibility and reduces waist circumference in CCS compared with the usual-care group after completion of the exercise program and at a 6-month follow-up. No significant changes in isometric back strength, hip circumference, body fat percentage, or muscle mass were found.
The primary finding of this randomized controlled trial is that participants exhibited a large effect size and a significant improvement in isometric abdominal strength after the CO-CUIDATE program. These results are consistent with a previous study investigating the stabilization of deep abdominal muscles in breast cancer survivors (8). CCS exhibit alterations in abdominal deep muscles of more than 50% relative to healthy controls (31), high levels of lower-back pain, and muscle hyperalgesia up to 6 months after surgery (32). However, we have not found any previous studies that report improvement in abdominal isometric strength despite improvement in muscle strength using other exercise modalities in CCS (35). One plausible explanation for our positive results is that CO-CUIDATE was performed under the supervision of two physiotherapists with an expertise in oncological rehabilitation who encouraged the patients during the exercises and ensured that each patient correctly executed the exercise program. Furthermore, all exercise prescriptions (intensity, sets, and repetitions) were generated based on individual capabilities, which is a relevant requirement of exercise programs to achieve better success. The changes found in this study support the possible inclusion of lumbopelvic stabilization exercises in supportive physical exercise guides for colon cancer.
The CO-CUIDATE program resulted in large improvements in functional capacity and flexibility. The gain of functional capacity is an important result of our trial (CO-CUIDATE group = 79.7 m vs control group = 4.9 m), and an improvement in walking distance of 54 m is clinically relevant (26). Our results demonstrated improvements in muscle strength and control that produced functional improvements, although the program was not specifically designed to improve functional capacity. These results are consistent with the results found by Yuen et al. (40) in breast cancer survivors. These researchers demonstrated that a 12-wk exercise program performed at home increased functional capacity to a greater extent when using resistance training (36.1 m) than when using an aerobic program (11.5). These results may be due to the selection of resistance exercises and improvements in the muscular state to increase function and improve cardiorespiratory capacity. Functional capacity is a very important modifiable risk factor after colorectal surgery (18), and it should be considered in all support strategies in CCS. The benefits observed in functional capacity after participation in the 8-wk CO-CUIDATE program were maintained 6 months later (large size effect), demonstrating that supportive strategies of physical activity are needed to improve health-related fitness in colon cancer patients. Although the CO-CUIDATE program did not focus on the improvement of functional capacity, functional capacity was improved.
The CO-CUIDATE participants exhibited a similar performance in the flexibility test as healthy subjects in a previous study (31), but these values were below the standard values for adults (2.1 cm for women and 0.6 cm for men) (15). A probable explanation for this difference is that CCS suffer abdominal pain after cancer treatment (32) because of illness and that they experience more difficulty in performing trunk flexion. The inactivity experienced by cancer patients because of treatment side effects may also lead to reduced physical functionality, which may explain the differences between the studies. Our results suggest that the CO-CUIDATE program resulted in positive effects on the health-related fitness, which usually decreases, of colon cancer patients (31). Our results showing changes in flexibility were influenced by age because physical fitness naturally decreases with age.
Isometric back strength was also improved after the CO-CUIDATE program, but these results were not significant. Strength exercises effectively improve lumbar extension muscle activity when the pelvis is stabilized (36). CCS suffer muscle alterations after interventions (11,31,32) and experience lumbar pain and widespread hyperalgesia pressure pain in their muscles (32). These results support the need for physical activity programs that include stabilization exercises in CCS.
We also found significant differences after the CO-CUIDATE program in waist circumference, with a large effect size, which is an important finding because abdominal obesity is a greater predictor of colon cancer risk than general obesity (19). Our improvements are consistent with more specific and longer lifestyle modification programs (3,35) and programs that include dietary changes (3). Bourke et al. (3) used a 12-wk lifestyle program with a greater volume of work per week as a method to further guide weight loss or control (30 min of aerobic exercise and two or four sets of 8 to 12 repetitions along with dietary recommendations). The CO-CUIDATE program obtained similar results in less time and with a lower exercise volume and less specific weight loss management. Similar previous studies also found a reduction in waist circumference (6), but we did not find any studies that used stabilization exercise programs in CCS. Therefore, our CO-CUIDATE program may provide adequate support for reducing the risk of colon cancer through a decrease in waist circumference and a reduction in mortality (2). Future studies using this exercise modality combined with dietary recommendations to maximize the effectiveness of both strategies on body composition in CCS, which is the primary objective in this population, are warranted.
The limitations of the trial include the fact that the CO-CUIDATE program may require significant resources for implementation. Two specialists led the exercise program, which is a significant cost over time. Another limitation is the enrollment of patients with a tumor between stage I and IIIa in a single hospital. Therefore, our participants could have some specific characteristics that make extrapolation of our results difficult. To the best of our knowledge, this study is the first randomized trial to demonstrate the benefits of a physical exercise program using the stabilization of deep abdominal muscles in CCS, and the results provide evidence of the necessity of a physical activity program in the rehabilitation of CCS. Few studies have examined the short- and long-term effects of a physical exercise program based on stabilization exercises in cancer patients (12,20,38), and no studies have investigated exercise in CCS. Another strength of the study is the high adherence rate and the low dropout rate. The adherence of the CO-CUIDATE group (88.36%) may be explained by the encouragement of oncologists to participate (24). This adherence was similar to another supervised physical exercise intervention with CCS (90%) (3), although it is slightly lower than adherence to exercise by patients with other types of cancer (95%) (25).
In conclusion, the CO-CUIDATE program, which is an 8-wk physical activity program based on stabilization exercises, is a promising strategy for improving health-related fitness and reducing waist and hip circumferences in CCS. These results are evident in the short and long term.
- An exercise program based on lumbopelvic exercise improves the control of deep abdominal muscles and health-related fitness.
- An exercise program based on lumbopelvic exercise is adaptable to individual capabilities.
- The CO-CUIDATE program does not require expensive material.
The authors acknowledge the patients for their participation, and they are also grateful to the Sporting Activities Centre of the University of Granada. This study was supported by a grant from the Education Ministry and Economy, Innovation, Science and Employment Counseling through the University of Granada CEI-BioTic. The authors declare no conflict of interest. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
TRIAL REGISTRATION: Clinical Trials.gov NCT02052050 (available in https://clinicaltrials.gov/ct2/show/NCT02052050?term=cantarero+villanueva&rank=1).
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