Effects of Aerobic and Resistance Training on Body Composition and Physical Capacity Of

55 Journal of Exercise Physiologyonline

April 2017 Volume 20 Number 2

Editor-in-ChiefOfficial Research Journal of the JEPonline TommyAmerican Boone, Society PhD, of MBA Exercise Review BoardPhysiologists Effects of Aerobic and Resistance Training on Body Todd Astorino, PhD Julien Baker,ISSN PhD1097-9751 Composition and Physical Capacity of Steve Brock, PhD Adolescents with Cystic Fibrosis Lance Dalleck, PhD Eric Goulet, PhD 1 2 Robert Gotshall, PhD Cristiano Queiroz de Oliveira , Vania de Matos Fonseca , Gilmar 3 3 4 Alexander Hutchison, PhD Senna , Estevão Scudese , Celia Regina de Miranda Chaves M. Knight-Maloney, PhD Len Kravitz, PhD 1Health Science Center, Catholic University of Petrópolis, Brazil, James Laskin, PhD 2Fernandes Figueira Institute, Department of Epidemiology, Brazil, Yit Aun Lim, PhD 3 Lonnie Lowery, PhD Nursing and Biosciences Post-Graduation Program, Doctorate of Derek Marks, PhD Federal University of State of Rio de Janeiro (UNIRIO), Brazil, Cristine Mermier, PhD 4Fernandes Figueira Institute, Department of Nutrition, Brazil Robert Robergs, PhD Chantal Vella, PhD ABSTRACT Dale Wagner, PhD Oliveira CQ, Fonseca VM, Senna G, Scudese E, Chaves CRM. Frank Wyatt, PhD Ben Zhou, PhD Effects of Aerobic and Resistance Training on Body Composition and Physical Capacity of Adolescents with Cystic Fibrosis. JEPonline 2017;20(2):55-63. The study investigated the effects of a 12-wk training program combining aerobic and resistance training on body composition and physical capacity of adolescents with cystic Official Research Journal of the American Society of fibrosis. The run/walk in treadmill program had duration of 23 min in Exercise Physiologists a moderate to high intensity. The resistance training consisted of 2 sets of 10 reps for the following exercises: lat pull down, leg press, ISSN 1097-9751 chest press, shoulder press, and sit-ups. The resistance training was performed with dumbbells and pulley machines. Before and after intervention, several evaluations were conducted: body composition by Slaughter`s equations, aerobic capacity by ergospirometry, and muscle endurance by push-up and sit-up tests. Significant increase in the fat free mass (P=0.01) was observed throughout the training period. Although the total body weight increased (P=0.02), no change was found in fat mass (P=0.24). Maximum oxygen uptake (P=0.03) and abdominal muscle endurance (P=0.04) were also significantly improved. Thus, the findings indicate that a supervised exercise program combining aerobic and resistance exercises significantly improved body composition, aerobic capacity, and abdominal muscle endurance in adolescents with cystic fibrosis.

Key Words: Exercise, Quality of Life, Adolescent Health Services 56

INTRODUCTION

Cystic fibrosis (CF) is an autossomic genetic disease that mainly affects the lungs and digestive tract (15). The lung disease is progressive with variable intensity (19) that may lead to airway obstruction and decreased lung function that generally gets worse as the patient grows older (10). Moreover, the lung inflammation may lead to diminished muscle function and a poor nutritional state (13). The bad absorption and digestion of lipids, proteins, and carbohydrates can also lead to a reduction in the patient’s body weight (19).

The lung disease and the loss of muscle mass are responsible for the increase in dyspnea and the early onset of muscle fatigue during exercise. As a consequence, physical fitness progressively decreases, which is associated with a further decrease in regular exercise. This vicious circle of negative events influences the overall quality of life (6). For this reason, given that regular exercise increases well-being, physical training is often acknowledged as a complementary strategy in the treatment of children and adolescents with CF.

The benefits of aerobic training and strength training, performed separately by children and adolescents with CF have been previously investigated (1,2,12,15,19,22,23,26). But, there is possibility that a combination of the two exercise modalities may be the best training program (1). However, while the scientific literature presents many studies evaluating aerobic exercise (3,8,9,12,18,19), there are just three studies that have analyzed exercise programs with resistance training (1,12,17) and none have utilized aerobic exercise with resistance exercises in the same training session.

Thus, the purpose of the present study was to investigate the effects of a 12-wk supervised exercise program on aerobic capacity, muscle endurance, and body composition of patients with CF aged from 10 to 16 yrs. We hypothesized that an exercise program including resistance exercise and treadmill running during the same session will result in improvements in body weight, muscle endurance, and aerobic capacity.

METHODS

Subjects The subjects of the study were selected from a cohort of 116 patients with diagnosed CF in accordance with the consensus of the Cystic Fibrosis Foundation (26). In order to participate in this study, the subjects: (a) had to be between 10 and 18 yrs of age; (b) have a forced expiratory volume in one second (FEV1) ≥60% of predicted value; and (c) a body mass index (BMI) above the 10th percentile (2) (Table 1).

The eligible patients were invited to participate in the research study during the regular visits to the hospital between April and February of the following year. The characteristics of the subjects that participated in the study are presented in Table 1. Informed written consent was obtained from each patient’s responsible adult prior to participation in the study. The study was approved by the Institutional Ethics Committee. 57

Table 1. Characteristics of the Eight Adolescents with CF Submitted to Intervention.

Patients Characteristics 1 2 3 4 5 6 7 8

Age (yrs) 16 12 11 16 10 10 11 14 Skin color B W B B B W W B Shwachman Score 67/75 62/75 70/75 70/75 50/75 70/75 65/75 75/75 Microbiology BC/PA/SA BC/PA/SA PA/SA PA BC/PA SA PA/MRSA PA FEV1 (% of 116.1% 87.6% 118% 95.1% 60.1% 92% 84.1% 117.9% predicted) Bronchiectasis Y Y Y Y Y N Y N Peribronchial N Y N N N Y N N thickening Mucoid impaction N Y Y N Y N N Y Air trapping N N N N Y Y N Y Mosaic perfusion N N Y Y N Y N N Pulmonary N N N N N N N N Hypertension Pancreatic Y Y Y Y Y Y Y Y Insufficiency Diabetes mellitus Y Y N N N N N N Liver disease Y N N N N N N N Sexual maturation P P PP P PP PP PP P Physiotherapy N 2 N 1 1 3 2 N

Y = Yes; N = No; B = black skin color; W = white skin color; Microbiology: BC = Burkholderia cepacia; PA = Pseudomonas aeruginosa; SA = Staphyloccocus aureus; MRSA = Methicillin resistant staphylococcus aureus; FEV1 (% of predicted) = forced expiratory volume in 1 sec (percentage of the predict for height and age); Sexual maturation: P = puber; PP = prepubescent

Measurements All subjects had anthropometric and physical fitness variables assessed in one visit before the beginning of exercise program. Fat free mass and fat mass were obtained by Slaughter’s equations (24) utilizing triceps and subscapular skinfolds assessed by Lange™ skinfold fat caliper according to standard techniques. The Lange™ skinfold fat caliper are manufactured by Cambridge Scientific Industries, Cambridge, Maryland, USA (24). Cardiopulmonary exercise testing (CPET) was used to determine the subjects’ maximal aerobic capacity (VO2 max) and maximal heart rate. The protocol consisted of a ramp cardiopulmonary exercise on a treadmill. Breath by breath gas exchanges were quantified by a TEEN 100 analyzer -1 (Aerosport™, Ann Arbor, USA). The VO2 data were expressed in absolute (L·min ) and relative values in relation to the subject’s body weight (mL·kg-1·min-1) and fat free mass (mL·FFM-1·min-1).

Abdominal muscle endurance was assessed by the total number of sit-ups performed during 1 min. The subject lay supine on a mat with the elbow joints in the extended position with the hands resting on the thighs while the knees were flexed at 90° that allowed for the feet to be flat on the mat 10 cm apart. The test instructor applied pressure to the subjects’ feet to keep them flat on the mat. A sit-up was correctly performed when the subject raised and touched the knees with the fingers while the elbows remained in the extended position. The subjects were instructed to do the sit-ups as fast as possible. The arm/shoulder muscle strength was 58 measured with push-ups. The subject was in the prone position on a mat, the hands placed at shoulder width apart under the shoulder joints with the fingers forward, arms straight, head and body aligned, and toes on the mat 10 cm apart. The push-up was correctly performed when the subject flexed the elbows to 90°, holding the body straight, which was followed by full elbow extension. When exhaustion occurred or if two incorrect push-ups were performed, the test was interrupted. The total number of correct push-ups was recorded.

Exercise Program Aerobic training consisted of a 15-min continuous walk/run on treadmill with the intensity fixed between 70% and 85% of each subject’s maximum heart rate obtained from the maximal cardiopulmonary exercise test. Prior and following the aerobic session, a 4-min warm-up and 4-min cool down were applied. In the first 2 wks of training, the sessions were designed to be shorter and with reduced intensity until the subjects were ready to perform the complete session. Resistance training (RT) consisted of 2 sets of 10 reps in the following exercises: lat pull down, leg press, chest press, shoulder press, and sit-ups using dumbbells and pulley machines. The workload was defined according the subject’s perceived effort as evaluated by the Borg CR-10 Scale (16). During the first 2 wks, the subjects were told to maintain an effort of 2 in the CR-10 Borg scale. The training volume and the intensity increased until the levels of 3 and 4 of the referred scale were reached.

Study Design All the subjects of the study performed aerobic and resistance exercises in the same training session 2 times a week during the 12-wk period. Each subject was individually supervised by a trained professional instructor. The acute change scoring system (25) was applied weekly by a pulmonologist in order to know whether the subjects could continue or should stop the exercise program.

Statistical Analyses

Univariate analysis failed to show the assumption of data normality. Therefore, possible within-group differences were tested by the Wilcoxon test. Statistical significance level was set at P≤0.05. All statistical calculations were performed using the SPSS 21.0 software (IBM™, Chicago, USA).

RESULTS

Twenty-one subjects were eligible for the study. However, two subjects did not attend the regular visits to the hospital during the invitation period and a third subject died during the same period. Thus, 18 adolescents were initially eligible to take part in the study. Nine of the 18 potential subjects refused to participate due to financial problems and another one abandoned the exercise program because of an accident. As a result, the subjects consisted of 8 adolescent. Four males and 4 females completed the intervention protocol (Figure 1). The mean FEV1 of the subjects was 96.4% ± 20.3% of the predicted value and the mean Shwachman score was 66.8/75 (SD = ± 9.6). The mean age of the group was 12.4 ± 2.5 yrs of age.

Table 2 presents compared results between pre- and post-training. A significant increase in the fat free mass (P = 0.01) was observed throughout the training period. Although the total 59 body weight increased (P = 0.02), no change was found in fat mass (P = 0.24). Also, the subjects’ maximum oxygen uptake (P = 0.03) and abdominal muscle endurance (P = 0.04) improved significantly.

Table 2. Data from Patients, Evaluated Prior and After the Period of Intervention.

Data Before Intervention After Intervention P (Means ± SD) (Means ± SD) value

Weight (kg) 42.1 ± 13.2 44.3 ± 13.6 0.02 Height (cm) 149.2 ± 11.9 151.2 ± 11.7 0.03 BMI (kg·m-2) 18.5 ± 3.1 18.9 ± 3.4 0.18 FFM (kg) 33.9 ± 9.6 35.6 ± 9.6 0.01 FM (kg) 8.0 ± 5.3 8.7 ± 5.7 0.24 -1 VO2 max (L·min )* 1.8 ± 0.7 2.1 ± 0.7 0.01 -1 -1 VO2 max (mL·kg ·min )* 44.1 ± 9.2 47.5 ± 8.7 0.03 -1 -1 VO2 max (mL·FFM ·min )* 53.9 ± 8.9 57.3 ± 7.4 0.09 Treadmill final speed (miles·hr-1)* 6.4 ± 1.2 7.0 ± 1.2 0.10 Maximum distance (km)* 1.8 ± 0.2 2.2 ± 0.6 0.04 Total exercise time (min)* 10.3 ± 2.6 11.8 ± 2.5 0.04 Total number of sit-ups (1 min) 50.0 ± 11.5 61.5 ± 9.4 0.04 Total number of push-ups 14.0 ± 6.9 17.5 ± 6.8 0.11

BMI = body mass index; FFM = fat free mass; FM = fat mass; AMC = arm muscle circumference; VO2 max -1 -1 -1 (L·min ) = maximum absolute oxygen uptake; VO2 max (mL·kg ·min ) = maximum oxygen uptake in values -1 -1 related to total mass; VO2 max (mL·MLG ·min ) = maximum oxygen uptake value related to fat free mass. *cardiopulmonary test data

DISCUSSION

The present study aimed to evaluate the effects of an exercise program of moderate intensity on the body composition, aerobic capacity, and muscle endurance. The main results were the increases in FFM, VO2 max, and in abdominal muscle endurance. Previous studies indicated that patients with a mild airway obstruction may engage in different modalities of exercise training (8). Even highly training endurance sports, such as marathon can be performed by trained adolescents with cystic fibrosis (4,7). Unfortunately, just a few patients with CF take part in exercise programs (21).

The available studies that investigated the effects of physical training as a complementary therapeutic strategy to adolescents with CF have usually applied just one kind of exercise per session of training. Orenstein et al. (12) and Selvadurai et al. (20) compared aerobic versus resistance training in two different groups of patients. Orenstein et al. (12) in another study utilized jogging or walking exercises. Straus et al. (26) were the first to employ resistance exercises for CF patients, and Gulmans et al. (8) opted to study stationary bike exercises. The present study is probably the first that applied an exercise protocol including aerobic and 60 resistance training in concurrent sessions, showing that significant and favorable changes in the overall physical fitness and body composition can be elicited by this kind of training.

Body Composition Adaptations

Aerobic exercise has not been shown to result in a weight gain in CF patients (1). Since this is one of the main goals in the clinical management of these patients (19), the present study included the resistance training as a strategy to increase the overall body mass (17). Strauss et al. (26) applied a resistance training program to 9 adult patients for 6 months. They observed a significant increase in the subjects’ weight (~2.88 kg). Selvadurai et al. (20) reported a 2.79 kg increase of the body mass in 18 children and adolescents after 3 wks of resistance training in a hospital facility, which was part of the treatment for pulmonary exacerbation. Similarly, Orenstein et al. (12) observed a mean weight gain of 4.6 kg in 28 children and adolescents who performed resistance training for 1 yr. The mean weight gain of the 8 subjects in the present study was 2.2 kg after a 12-wk exercise program that included resistance exercises, which seems to concur with the previous findings.

The increase of FFM was probably the main cause for the weight gain found in our study, since no difference was observed for the fat mass assessed by the skinfolds method. It is therefore possible that there is a relationship between the gain weight in the CF subjects and muscle development induced by the resistance training. In this sense, there is accumulated evidence associating the weight gains in CF patients engaged in resistance training to an increase of the insulin growth factor (IGF) secretion. The IGF is one of the active hormones for protein metabolism, and the increased concentration leads to decreased protein degradation with a consequent increase of fat free mass and weight gain (3). The increase of FFM is important for two reasons. First, it represents muscle gain (including the chest wall muscles), which may improve the breathing capacity. Second, subjects with CF usually loose muscle mass because of a higher protein catabolism, which is one of the main determinants of effort tolerance limitation (11).

Physical Capacity Adaptations

Physical fitness was evaluated by cardiopulmonary exercise testing and resistance exercises. Both absolute and relative VO2 max increased. Selvadurai et al. (20) observed an increase of 21.6% in VO2 max of children and adolescents in hospital-based treatment, which performed aerobic training over a 3-wk period. Orenstein et al. (12) observed that the children and adolescents with CF who performed home-based aerobic exercise during a year maintained their aerobic capacity, whereas patients that did not engage in aerobic training exhibited a significant decrease of VO2 max.

In the present study, there was an increase of 7.7% in VO2 max, which is somewhat lower than the findings in previous studies. This difference between the results may be due to the greater baseline VO2 max observed in our subjects compared to those from the study by Selvadurai et al. (20) (44.1 mL·kg-1·min-1 vs. 33.8 mL·kg-1·min-1, respectively). Another difference between both studies was the FEV1 in baseline (96.7% of predicted vs. 56.8% of predicted, respectively), which indicates that the clinical conditions of our subjects was better compared to the subjects in the study by Selvadurai et al. (20). The influence of baseline fitness on the aerobic gains in the present study can be illustrated by the fact that two of the 61 three patients that presented the worst initial aerobic capacity exhibited the greater increases -1 -1 in VO2 max (7.5 and 7.8 mL·kg ·min ). The other patient that did not increase VO2 max to the same extent presented the worst clinical condition at baseline (Shwachman score of 50/75 and FEV1 of 60.1% of predicted) and the worst prognostic result after the study. There was also a significant increase in the mean total test duration and final treadmill speed. These results suggest that the ability to perform daily tasks improved as a general effect of the exercise protocol.

The abdominal muscle endurance increased significantly. The development of the abdominal and thoracic muscle region is important to patients with CF, given that it has a direct impact on breathing capacity. The results of some previous research concur with these findings and strongly suggest that patients with CF can respond favorably to moderate strength training (2,12). Such evidence should be considered in the treatment of patients with CF, which is especially true for adolescents, since they are usually interested in these kinds of exercises and they exhibit higher adherence to programs that combine aerobic and resistance training rather than programs that contain just aerobic sessions (17).

Limitations of this Study

One of the main limitations of the present study was the lack of a control group and the small sample size. A factor that contributed for these problems was the distance between the subjects’ homes and the hospital where the training routines took place. It would be advantageous in this context to develop home-based training programs adapted to CF patients in order to maximize the potential effects of exercising on their functional capacity and clinical condition. Unfortunately, there are very few studies investigating the effects on unsupervised exercise programs in patients with CF and the results are somewhat discordant (9,19). Further research is warrant to address this issue.

CONCLUSIONS

Overall, the present results strongly suggest that physical training programs combining aerobic and resistance exercise can significantly improve body composition and physical fitness of patients with CF. Thus, children with CF should be encouraged to exercise regularly as a paramount part of their treatment.

Address for correspondence: Gilmar Senna, Federal University of State of Rio de Janeiro, Xavier Sigaud Street- 290 - 401 - Praia Vermelha, 22290-180, Rio de Janeiro, RJ, Brazil. E- mail: [email protected]

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