published ahead of print effectiveness of lumbopelvic...

. . . Published ahead of Print

Medicine & Science in Sports & Exercise® Published ahead of Print contains articles in unedited manuscript form that have been peer reviewed and accepted for publication. This manuscript will undergo copyediting, page composition, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered that could affect the content.

Copyright © 2016 American College of Sports Medicine

Effectiveness of Lumbopelvic Exercise in Colon Cancer Survivors

Irene Cantarero-Villanueva

1,2,3, Antonio Sánchez-Jiménez

3, Noelia Galiano-Castillo

3,

Lourdes Díaz-Rodríguez1,2,4

, Lydia Martín-Martín3, and Manuel Arroyo-Morales

1,2,3

1Institute for Biomedical Research ibs, Granada, Spain

2Mixed University Sport and Health Institute, iMUDS University of Granada, Spain

3Department of Physical Therapy, Health Sciences Faculty, University of Granada, Spain

4Department of Nursing, Health Sciences Faculty, University of Granada, Spain

Accepted for Publication: 22 February 2016

ACCEPTED

Copyright © 2016 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

Effectiveness of Lumbopelvic Exercise in Colon Cancer Survivors

Irene Cantarero-Villanueva1,2,3

, Antonio Sánchez-Jiménez3, Noelia Galiano-Castillo

3, Lourdes

Díaz-Rodríguez1,2,4

, Lydia Martín-Martín3, and Manuel Arroyo-Morales

1,2,3

1Institute for Biomedical Research ibs, Granada, Spain

2Mixed University Sport and Health Institute, iMUDS University of Granada, Spain

3Department of Physical Therapy, Health Sciences Faculty, University of Granada, Spain

4Department of Nursing, Health Sciences Faculty, University of Granada, Spain

* Corresponding author: I. Cantarero-Villanueva

Department of Physical Therapy, Health Sciences Faculty, University of Granada, Parque

Tecnológico de la Salud. Avenida de la Ilustración,60 18016 Granada, Spain

Email address: [email protected]

Phone: +34958248764

Fax: +34 958 24 20 70

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 results

of the present study do not constitute endorsement by the ACSM.

CONFLICT OF INTEREST: None declared.

Running title: Lumbopelvic exercise in cancer survivors

Medicine & Science in Sports & Exercise, Publish Ahead of PrintDOI: 10.1249/MSS.0000000000000917

ACCEPTED


ABSTRACT

Introduction: This study evaluated the effectiveness of lumbopelvic exercise in improving

health-related fitness, anthropometric measurements and body composition in colon cancer

survivors (CCS).

Methods: Forty-six CCS (35% female, n=14) were assigned to two groups for this randomized

controlled clinical trial: a trunk muscle stabilization exercise program group (CO-CUIDATE)

and a usual-care group. The CO-CUIDATE program was conducted for 8 weeks (3 times per

weeks). The primary endpoint was isometric abdominal strength measured using the trunk curl

test. The secondary endpoints used were isometric back strength, functional capacity, lower-body

flexibility, weight and anthropometric measurements evaluated at baseline, after the physical

exercise program and after 6 months of follow-up. A trained member of the research group with

5 years of experience working with cancer patients and who was blinded to the patient group

assessed the variables. All physical tests were carried out with multiple observations.

Results: The adherence to intervention was 88.36%, and 2 drop-outs (10.5%) were recorded.

Minor side effects, including discomfort with the exercises in the first sessions, were reported by

the participants. ANOVA demonstrated significant differences in group x time interactions for

isometric abdominal strength (F= 7.7; p= 0.001), functional capacity (F= 4.6; p= 0.015), lower-

body flexibility (right, F= 4.3, p= 0.021 and left, F= 3.6, p= 0.034) and waist circumference (F=

5.7; p= 0.07), which were the best values for the CO-CUIDATE group. No significant changes in

isometric back strength, weight, hip circumference or body composition were observed.

Conclusion: An 8-week program based on stabilization exercises is a promising strategy to

increase health-related fitness and reduce waist circumference in CCS. An exercise program

ACCEPTED


based on lumbopelvic exercise is a feasible intervention to improve the control of deep

abdominal muscles and health-related fitness.

KEYWORDS: colon cancer survivorship, health related fitness, anthropometric, physical

activity, stabilization exercise program

TRIAL REGISTRATION: Clinical Trials.gov NCT02052050 (available in

https://clinicaltrials.gov/ct2/show/NCT02052050?term=cantarero+villanueva&rank=1)

ACCEPTED


INTRODUCTION

Colorectal cancer is the cause of 13% of cancer deaths (13). The survival rate 5 years 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

ACCEPTED


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 (7,5), 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 (ACSM) 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 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

ACCEPTED


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 endpoints compared with the effects of the usual-care protocols.

METHODS

SUBJECTS:

For this randomized controlled clinical trial, 46 CCS (35% female, n=14) were assigned to one

of two groups within one year 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

years old, (2) received curative treatment due to cancer (surgery, chemotherapy and/or

radiotherapy), (3) were diagnosed with grades I to III A of colorectal cancer and (4) completed

coadjuvant treatment. Subjects were excluded if they presented cancer recurrence, underwent

previous abdominal surgeries or were diagnosed with concomitant conditions, such as previous

lower-back pain or musculoskeletal conditions (e.g., osteoarthritis, fibromyalgia or chronic

fatigue syndrome).

ACCEPTED


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 seconds in the post-treatment

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 seconds. Each group included 18 participants. We chose 23

participants for each group assuming a 20% drop-out 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.

ACCEPTED


INTERVENTION:

Two physiotherapy experts in oncological rehabilitation with more than 7 years of experience

working with oncology patients performed the CO-CUIDATE program, which was conducted in

90 minute sessions 3 times per weeks for 8 weeks. Each session included warm-up exercises (10

to 20 minutes), core stabilization exercises (20 to 30 minutes) 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 Rating of Perceived Exertion 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 drop-outs if they did not participate

in at least 75% (18) 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 weeks 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.

ACCEPTED


ENDPOINTS AND MEASUREMENTS

Health-related fitness endpoints

The primary outcome was isometric abdominal strength, which was assessed using the trunk curl

test. Patients remained in a supine position with a 90-degree 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 seconds. This test exhibits an intraclass

correlation coefficient (ICC) > 0.97 (22).

Secondary endpoints

1. Physical endpoints

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 30º, 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 minutes. 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).

ACCEPTED


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 carried out with multiple observations.

2. Anthropometric endpoints

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 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 years of experience in taking these measurements

on cancer patients and who was blinded to patient group assessed these variables at the three

ACCEPTED


time points. Measurements were performed in the physiotherapy laboratory of the Faculty of

Health Sciences at the University of Granada (Spain).

STATISTICAL ANALYSIS

Mean, coefficient intervals (confidence level, 95%) and standard deviations were used in

descriptive analyses. Student’s t and chi-square tests 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, post-program 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 determine if 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 (ITT) The worst-case value was used to replace

missing data, following a previously reported procedure (30).

ACCEPTED


RESULTS

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 drop-outs are also shown. There were 2 drop-outs (10.5%)

in the CO-CUIDATE group (reasons: never started the program, n=1; too busy, n=1) and 4 drop-

outs (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 one week

because he suffered a peripheral neuropathy. The average range of the perception of fatigue was

12 (6-17).

Health-related fitness endpoints

ANOVA revealed a significant difference (F= 7.7, p= 0.001) in the group x time interaction for

isometric abdominal strength. The CO-CUIDATE group experienced a greater increase in

ACCEPTED


isometric abdominal strength compared with that of the usual-care group after discharge (table

4). The intergroup effect size was large after the 8-week 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 non-significant trend for the group x time interactions, with a greater increase in

the CO-CUIDATE group compared with that in the usual-care group (table 4).

Physical endpoints analyses:

Statistical analyses revealed significant differences in group x 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 endpoint analyses

A significant group x 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;

ACCEPTED


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 x time interactions for the

variables of hip circumference, weight or body composition.

DISCUSSION

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

ACCEPTED


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 meters vs. control group = 4.9 meters), and an improvement in walking distance of

54 meters is clinically relevant (26). Our results demonstrated improvements in muscle strength

and control that produced functional improvements, even though the program was not

specifically designed to improve functional capacity. These results are consistent with the results

found by Yuen and collaborators (40) in breast cancer survivors. These researchers demonstrated

that a 12-week exercise program performed at home increased functional capacity to a greater

extent when using resistance training (36.1 meters) 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-week CO-CUIDATE program were maintained six 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.

ACCEPTED


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 (35, 3) and programs that include

dietary changes (3). Bourke and collaborators (3) used a 12-week lifestyle program with a

ACCEPTED


greater volume of work per week as a method to further guide weight loss or control (30 minutes

of aerobic exercise and 2 or 4 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

ACCEPTED


participate (24). This adherence was similar to another supervised physical exercise intervention

with CCS (90%) (3), though 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-week 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.

CLINICAL IMPLICATIONS:

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.

ACCEPTED


ACKNOWLEDGMENTS

The authors acknowledge the patients for their participation, and we 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 results of the present study do not constitute

endorsement by the ACSM.

CONFLICT OF INTEREST AND SOURCE OF FUNDING

None declared.

ACCEPTED


REFERENCES

1. Altman DG. Practical Statistics for Medical Research. London: Chapman & Hall;

1991.396-435 p.

2. Argilés JM, Busquets S, Stemmler B, López-Soriano FJ. Cachexia and sarcopenia:

mechanisms and potential targets for intervention. Curr Opin Pharmacol.

2015;22:100-106.

3. Bourke L, Thompson G, Gibson DJ, et al. Pragmatic lifestyle intervention in patients

recovering from colon cancer: a randomized controlled pilot study. Arch Phys Med

Rehabil. 2011;92(5):749-55.

4. Broskey NT, Greggio C, Boss A, et al. Skeletal muscle mitochondria in the elderly:

effects of physical fitness and exercise training. J Clin Endocrinol Metab.

2014;99(5):1852-61.

5. Bullo V, Bergamin M, Gobbo S, et al. The effects of Pilates exercise training on

physical fitness and wellbeing in the elderly: A systematic review for future exercise

prescription. Prev Med. 2015;75:1-11.

6. Cakmakçi O. The effect of 8 week pilates exercise on body composition in obese

women. Coll Antropol. 2011;35(4):1045-50.

7. Campos de Oliveira L, Gonçalves de Oliveira R, Pires-Oliveira DA. Effects of Pilates

on muscle strength, postural balance and quality of life of older adults: a randomized,

controlled, clinical trial. J Phys Ther Sci. 2015;27(3):871-6.

8. Cantarero-Villanueva I, Fernández-Lao C, Cuesta-Vargas AI, Del Moral-Avila R,

Fernández-de-Las-Peñas C, Arroyo-Morales M. The effectiveness of a deep water

ACCEPTED


aquatic exercise program in cancer-related fatigue in breast cancer survivors: a

randomized controlled trial. Arch Phys Med Rehabil. 2013;94(2):221-30.

9. Carbonell-Baeza A, Álvarez-Gallardo IC, Segura-Jiménez V, et al. Reliability and

feasibility of physical fitness tests in female fibromyalgia patients. Int J Sports Med.

2015;36(2):157-62.

10. Cohen J. A power primer. Psychological Bulletin. 1992;112: 155-159.

11. DuBay DA, Choi W, Urbanchek MG, et al. Incisional herniation induces decreased

abdominal wall compliance via oblique muscle atrophy and fibrosis. Ann Surg.

2007;245(1):140-6.

12. Eyigor S, Karapolat H, Yesil H, et al. Effects of pilates exercise on functional

capacity, flexibility, fatigue, depression and quality of life in female breast cancer

patients: a randomized controlled study. Eur J Phys Rehabil Med. 2010;46(4):1–7.

13. Global Health Observatory of the World Health Organization Web site [Internet].

Ginebra: World Health Organization; [cited 2015 May 14]. Available

from:http://www.who.int/gho/en/.

14. Gruther W, Wick F, Paul B, et al. Diagnostic accuracy and reliability of muscle

strength and endurance measurements in patients with chronic low back pain. J

Rehabil Med. 2009;41(8):613-9.

15. Kirkham AA, Neil-Sztramko SE, Morgan J, et al. Health-related physical fitness

assessment in a community-based cancer rehabilitation setting. Support Care Cancer.

2015;e25617069.

ACCEPTED


16. Klimentidis YC, Bea JW, Lohman T, Hsieh PS, Going S, Chen Z. High genetic-risk

individuals benefit less from resistance exercise intervention. Int J Obes (Lond).

2015;e25924711.

17. Latey P. The Pilates method: history and philosophy. J Bodyw Mov Ther.

2001;5(4):275-82.

18. Li C, Carli F, Lee L, et al. Impact of a trimodal prehabilitation program on functional

recovery after colorectal cancer surgery: a pilot study. Surgical

Endoscopy.2013;27:1072–82.

19. MacInnis RJ, English DR, Hopper JL, Gertig DM, Haydon AM, Giles GG. Body size

and composition and colon cancer risk in women. Int J Cancer. 2006;118(6):1496–

1500.

20. Martin E, Battaglini C, Groff D, Naumann F. Improving muscular endurance with the

MVe Fitness Chair™ in breast cancer survivors: a feasibility and efficacy study. J Sci

Med Sport. 2013;16(4):372-6.

21. McGill SM, Childs A, Liebenson C. Endurance times for low back stabilization

exercises: clinical targets for testing and training from a normal database. Arch Phys

Med Rehabil.1999; 80(8):941–944.

22. Meyerhardt JA, Heseltine D, Niedzwiecki D, et al. Impact of physical activity on

cancer recurrence and survival in patients with stage III colon cancer: findings from

CALGB 89803. J Clin Oncol. 2006;24(22): 3535-3541.

23. Otto SJ, Korfage IJ, Polinder S, et al. Association of change in physical activity and

body weight with quality of life and mortality in colorectal cancer: a systematic

review and meta-analysis. Support Care Cancer. 2015;23(5):1237-50.

ACCEPTED


24. Park JH, Lee J, Oh M, et al. The effect of oncologists' exercise recommendations on

the level of exercise and quality of life in survivors of breast and colorectal cancer: A

randomized controlled trial. Cancer. 2015; e 25965782.

25. Rajarajeswaran P, Vishnupriya R. Exercise in cancer. Indian Journal of Medical and

Paediatric Oncology : Official Journal of Indian Society of Medical & Paediatric

Oncology. 2009;30(2):61–70.

26. Redelmeier DA, Bayoumi AM, Goldstein RS, Guyatt GH. Interpreting small

differences in functional status: the Six Minute Walk test in chronic lung disease

patients. Am J Respir Crit Care Med. 1997;155:1278–82.

27. Renfro LA, Grothey A, Kerr D, et al. Survival following early-stage colon cancer: an

ACCENT-based comparison of patients versus a matched international general

population†. Ann Oncol. 2015;26(5):950-8.

28. Roberts BM, Frye GS, Ahn B, Ferreira LF, Judge AR. Cancer cachexia decreases

specific force and accelerates fatigue in limb muscle. Biochem Biophys Res Commun.

2013;435(3):488-92.

29. Rogers K, Gibson AL. Eight-week traditional mat Pilates training-program effects on

adult fitness characteristics. Res Q Exerc Sport. 2009;80(3): 569-74.

30. Rydeard R, Leger A, Smith D. Pilates-based therapeutic exercise: effect on subjects

with nonspecific chronic low back pain and functional disability: a randomized

controlled trial. J Orthop Sports Phys Ther. 2006;36(7):472-84.

31. Sánchez-Jiménez A, Cantarero-Villanueva I, Delgado-García G, et al. Physical

impairments and quality of life of colorectal cancer survivors: a case-control study.

Eur J Cancer Care (Engl). 2014;e 25055886.

ACCEPTED


32. Sánchez-Jiménez A, Cantarero-Villanueva I, Molina-Barea R, Fernández-Lao C,

Galiano-Castillo N, Arroyo-Morales M. Widespread pressure pain hypersensitivity

and ultrasound imaging evaluation of abdominal area after colon cancer treatment.

Pain Med. 2014;15(2):233-40.

33. Schmidt K, Vogt L, Thiel C, Jäger E, Banzer W. Validity of the six-minute walk test

in cancer patients. Int J Sports Med. 2013;34(7):631-6.

34. Schmitz KH, Courneya KS, Matthews C, et al. American College of Sports Medicine

roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc.

2011;43(1):1409-26.

35. Sellar CM, Bell GJ, Haennel RG, Au HJ, Chua N, Courneya KS. Feasibility and

efficacy of a 12-week supervised exercise intervention for colorectal cancer survivors.

Appl Physiol Nutr Metab. 2014;39(6):715-23.

36. Smith D, Bissell G, Bruce-Low S, Wakefield C. The effect of lumbar extensión

training with and without pelvic stabilization on lumbar strength and low back pain. J

Back Musculoskelet Rehabil. 2011;24(4):241-9.

37. Sonnenschein EG, Kim MY, Pasternack BS, Toniolo PG. Sources of variability in

waist and hip measurements in middle-aged women. Am J Epidemiol.

1993;138(5):301-9.

38. Stan DL, Rausch SM, Sundt K, et al. Pilates for breast cancer survivors. Clin J Oncol

Nurs. 2012;16(2):131-41.

39. Thomas EL, Frost G, Harrington T, Bell JD. Validation of ‘InBody’Bioelectrical

Impedance by Whole Body MRI. Laboratory Report [Internet]. 2001. [cited 2015

May 14];1-2p. Available from:

ACCEPTED


http://www.fysiotest.se/swe/InBody_Studier_files/R%20Steiner%20validation_1.pdf.

40. Yuen HK, Sword D. Home-based exercise to alleviate fatigue and improve functional

capacity among breast cancer survivors. J Allied Health. 2007;36(4):e257-75.

ACCEPTED


FIGURE LEGENDS

Figure 1. Study flow diagram

ACCEPTED


Figure 1

ACCEPTED


Table 1: Physical exercise program CO-CUIDATE.

Exercise

description

Volume and Intensity progression

Week

1

Week

2

Week

3

Week

4

Week

5

Week

6

Week

7

Week

8

Aerobic

exercise

Brisk

walking or

running

5+5

min

10+5

min

15

min

10+10

min

20

min

20+5min 20+5

min

10+10

min

Stabilization

Exercise

Program

Pilates

exercise

1 set

of 8-

10

reps

1 set

of 12

reps

2sets

of 8

reps

2 sets

of 10

reps

1 set

of 12

reps

2 sets of

12 reps

3 sets

of 8

reps

2 sets

of 10

reps

Local Segmental Control Exercise

Roll Up- Roll Down

One Leg Circle

Side Kicks

Saw

Hundred

Leg Pull Front

ACCEPTED


Stretching

exercise

Specific and general exercises. The progression was performed for the feelings

(not pain) and autonomy

Notes All therapeuticexercises were focused to breathing and specific muscles

activation (mind-body exercise) and were made with instructor assist.

Intensity of exercises was quantified on the Borg Rating of Perceived Exertion

(RPE) scale

ACCEPTED


Table 2: Demographic, clinical and medical characteristics of the groups.

Characteristic CUIDATE group

(n= 21)

Control group

(n= 19)

P-value

Age (year), mean (SD)* 57.5±8.0 62.3±7.9 0.066a

Gender n (%)

Male

Female

13 (61.9)

6 (38.1)

13 (68.4)

8 (31.6)

0.294 c

Time since diagnosis (month)

mean(SD)*

13.8±7.8 17.1±11.3 0.293 a

Time since intervention

(month) mean(SD)*

12.0 ±7.4 14.6±10.0 0.436 a

Marital status, n (%)

Married

Unmarried

Divorced

19 (90.5)

1 (4.8)

1 (4.8)

15 (78.9)

2 (10.5)

2 (10.5)

0.294 b

Tumor stage, n (%)

II

IIIa

7 (33.3)

14 (66.7)

7 (36.8)

12 (63.2)

0.539 b

Educational level, n (%)

Primary schooling

Secondary schooling

University

9 (42.9)

6 (28.6)

6 (28.6)

14 (73.7)

3 (15.8)

2 (10.5)

0.200 b

ACCEPTED


Type of surgery, n (%)

Right hemicolectomies

Left hemicolectomies

Sigmoid colectomies

Anterior resections

6 (28.6)

3 (14.3)

5 (23.8)

7 (33.3)

6 (31.6)

0

8 (42.1)

5 (26.3)

0.269 b

Tobacco

No

Yes

Ex-smoker

7(33.3)

2 (9.5)

12 (57.1)

13 (68.4)

2 (10.5)

4 (21.1)

0.057 b

Alcohol Intake

Never

Monthly

Weekly

Dialy

7 (33.3)

5(23.8)

7 (33.3)

2 (9.5)

8 (42.1)

4 (21.1)

2 (10.5)

5 (26.3)

0.169 b

Physical activity (METS/h-d)

mean(SD)*

4.2±2.1 4.1±2.6 0.940 a

*values mean ± SD are expressed as mean (95% confidence interval) or as number and

percentage. P values for inter-group comparisons using t-student (a) and chi-square (

b) test.

ACCEPTED


Table 3: Comparison of variables data between groups at baseline

*P < 0.05 **P < 0.001 for ANOVA analysis between groups.

CO-CUIDATE program

group

(n= 21)

Control

group

(n=19)

P value

Health-related fitness

Trunk curl test (sec) 25.3 ± 10.5 24.3 ± 11.6 0.71

Back dynamometer (kg) 62.2 ± 36.5 54.8 ± 25.1 0.21

6-min walk test (m) 330.8 ± 137.2 288.8 ± 132.3 0.83

Modified Sit and Reach test

(right, cm)

-9.2 ± 10.9 -10.4 ± 12.1

0.61

Modified Sit and Reach test

(left, cm)

-10.0 ± 11.0 -6.3± 13.4

0.30

Anthropometric outcomes

Waist Circumference (cm) 102.5 ± 13.6 101.1 ± 11.2 0.60

Hip Circumference (cm) 108.3 ± 02.4 108.6 ± 02,5 0.72

Weight (kg) 74.7 ± 10.8 76.4 ± 14.2 0.30

Body Fat (%) 34.9 ± 10.5 32.6 ± 9.2 0.55

Muscle Mass (kg) 26.9 ± 5.8 26.9 ± 5.2 0.51

Body Mass Index 28.4 ± 5.0 28.2 ± 5.0 0.97 ACCEPTED


Table 4: Pre-intervention, post-intervention, 6 months follow-up and change scores for mean

values ± standard deviation of health-related fitness.

CO-CUIDATE

program group

(n=21)

Control group

(n=19)

Between-Group

Differences

Trunk curl test (sec)

Pre-intervention 25.3 ± 10.5 24.3 ± 11.6

-26.0 (-39.2;-12.7)**

-7.2 (-7.2-21.8)

Post-intervention 54.0 ± 26.3 27.0 ± 12.6

6 months follow-up 42.0 ± 26.6 33.8 ± 23.9

Within Group Change

Scores

Pre-post intervention

Pre intervention- 6

months follow up

28.6 (17.4-39.9)

16.6 (4.2-29.6)

2.6 (-9.1-14.5)

9.4 (-3.6-22.4)

Back dynamometer (kg)


-4.6 (-16.2;-6.8)


6 months follow-up 71.3 ± 37.3 53.3 ± 23.2

Within Group

Change Scores

8.2 (-1.5-18.1)

3.6 (-6.7-13.9)

ACCEPTED



Pre intervention- 6

months follow up

9.1 (0.2-17.9)

-1.5 (-10.8-7.8)

-10.6 (-21.0-0,2)

6-min walk test (m)


-74.8 (-131.8;-17.3) *

-82.9 (-143.2;-22.6) *


6 months follow-up 393.3 ± 148.4 279.8 ± 119.8

Within Group

Change Scores


Pre intervention- 6

months follow up

79.7 (31.6-128.4)

62.4 (16.9-108.0)

4.9 (-46.2-56.0)

-8.9 (-56.8- - 38.9)

Modified Sit and Reach test (right, cm)

Pre-intervention -9.2 ± 10.7 -10.4 ± 12.1

-5.4 (-9.5;-1.4)*¥

-2.1 (-74.6-0.2)

Post-intervention -5.0 ± 10.9 -11.7 ± 11.8

6 months follow-up -7.7 ± 10.3 -11.1 ± 12.8

Within Group Change

Scores


4.2 (0.7-7.6)

-1.2 (-4.8-2.3)

-0.7 (-2.8-1.4)

ACCEPTED


Values are expressed as mean ± standard deviation for pre, post-intervention and 6 months

follow up data and as mean (95% confidence interval) for within- and between-group change

scores. * Significant group × time interaction (repeated ANCOVA test, P < 0.05). . **

Significant group × time interaction (repeated ANCOVA test, P < 0.001). . ¥ influenced by aged.

Pre intervention- 6

months follow up

1.4 (-0.6-3.5)

Modified Sit and Reach test (left, cm)

Pre-intervention -10.0 ± 11.0 -6.3± 13.4

-7.5 (-13.1;-2.0)*¥

-4.4 (-9.3;0.4)

Post-intervention -6.1 ± 11.2 -9.9 ± 10.0

6 months follow-up -8.8± 10.4 -9.5 ± 13.8

Within Group Change

Scores


Pre intervention- 6

months follow up

3.9 (-0.8-8.6)

1.2 (-2.9-5.4)

-3.6 (-8.6-1.1)

-3.2 (-7.6-1.1)

ACCEPTED


CO-CUIDATE

program group

(n=21)

Control group

(n=19)

Between-Group

Differences

Waist Circumference (cm)


5.1 (1.6:8.7) *

2.4 (0.1:4.6) *


6 months follow-up 103.0 ± 12.5 104.0 ± 11.1

Within Group

Change Scores


Pre intervention- 6

months follow up

-3.6 (-6.6:-0.5)

0.4 (-1.4:2.3)

1.5 (-1.6:-4.7)

2.9 (0.9:4.9)

Hip Circumference (cm)


2.4 (-0.4:04.5)

-0.5 (-2.4:1.4)


6 months follow-up 109.2 ± 13.4 108.9 ± 9.1

Within Group

Change Scores


Pre intervention- 6

-1.7. (-3.4; 00.0)

0.8 (-081:2.54)

0.7 (-0.0:3.4)

0.3 (-1.4:2.0)

ACCEPTED


months follow up

Weight (kg)


-0.2 (-3.1:2.6)

1.2 (-4.7:2.1)


6 months follow-up 79.3 ± 13.2 76.4 ± 11.3

Within Group Change

Scores


Pre intervention- 6

months follow up

1.2 (-1.2:3.7)

2.9 (0.0:5.8)

0.9 (-1.1:3.0)

1.6 (-1.3:4.7)

Body Fat (%)

Pre-intervention 34.9 ± 10.5 32.6± 9.2

1.5 (-0.1:3.3)

1.7 (-1.1:4.5)


6 months follow-up 35.7 ± 9.9 35.2 ± 8.6

Within Group Change

Scores


Pre intervention- 6

months follow up

-0.9 (-2.4:0.5)

0.8 (-1.5:3.2)

0.6 (-0.9:2.1)

2.5 (-0.0:5.1)

ACCEPTED


Muscle Mass (kg)


-0.8 (-2.1:0.3)

-0.8 (-2.1:0.4)


6 months follow-up 27.8± 5.6 26.9± 5.2

Within Group Change

Scores


Pre intervention- 6

months follow up

1.0 (-0.0:2.1)

0.9 (-0.1:2.0)

0.1 (-0.9:1.2)

0.0 (-1.6:1.2)

Body Mass Index


0.7 (0.6:0.8)

-0.3 (-1.3:0.6)


6 months follow-up 29.3 ± 4.6 28.8 ± 4.8

Within Group Change

Scores


Pre intervention- 6

months follow up

0.3 (-0.3:0.9)

0.9 (0.0.1.7)

0.3 (-0.2:1.0)

0.5 (-0.3:1.4)

ACCEPTED


Table 5: Pre-intervention, post-intervention, 6 months follow-up and change scores for mean

values ± standard deviation of anthropometric measurement.

Values are expressed as mean ± standard deviation for pre, post-intervention and 6 months

follow up data and as mean (95% confidence interval) for within- and between-group change

scores. * Significant group × time interaction (repeated ANCOVA test, P < 0.05). ** Significant

group × time interaction (repeated ANCOVA test, P < 0.001). ¥ influenced by aged.

ACCEPTED

published ahead of print effectiveness of lumbopelvic...

Documents