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Systems Physiology – Immune Function

Effect of 10-Week Long Resistance Training Program on the Acute Levels of Cytokines

NUNES JOÃO ELIAS DIAS1,2, DE AGOSTINI GUILHERME GULARTE1, NICIOLI CRISTIANE2, FERREIRA FABIANO CÂNDIDO2, BALDISSERA VILMAR 2, PEREZ SÉRGIO EDUARDO DE ANDRADE 2

1Laboratory of the Physiology of Performance/ Federal University of Uberlândia, Uberlândia, Brazil, 2Laboratory of the Physiology of Exercise/ Federal University of São Carlos, São Carlos, Brazil

ABSTRACT

Nunes JED, De Agostini GG, Nicioli C, Ferreira FC, Baldissera V, Perez SEA. Resistance Training Program and Cytokines Before and After the Completion of a Fatigue Test. JEPonline 2010;13(3):40-48. Evidence suggests that exercise can induce the production of cytokines. We evaluated the effect of a 10-week circuit resistance training program (CRTP) on the acute effect of two fatigue tests (FT), the bench press (BP) and the leg press at 45˚ (LP), on the plasma concentrations of IL-6, IL-8, IL-10, IL-1β, and TNF(. Volunteers took two FT, which were performed in three series with 50% of 1-RM done until exhaustion and 1-minute intervals between the series, before and after the CRTP. A total of 14 non-trained women, at 39.8±3.9 years, 60.6±6.6 kg and 163.6±6.6 cm, participated in the study. The plasma concentrations of IL-8 for the LP exercise, taken before and after the FT and from the pre- and post-training periods, were (Pre: 4.4±2.6 and 5.7±1.0 pg/ml, p = 0,333) and (Post: 6.4±1.3 and 6.5±2.1 pg/ml, p = 0,797), respectively. For the BP exercise, the levels were (Pre: 3.7±3.9 and 9.0±2.6 pg/ml, p = 0,057) and (Post: 5.7±2.1 and 7.1±2.3 pg/ml, p = 0,164). IL-6, IL-10, IL-1β, and TNF( did not reach the minimum limit of detection. Our data, then, support the idea that the two FT done do not provoke stress sufficient to alter the cytokinaemia.

Key Words: Immune Function, Fatigue, Bench Press, Leg Press, Women.

INTRODUCTION

Cytokines are pleiotropic proteins produced by potentially all nuclei of cells in the body.(20) Evidence suggests that exercise is an induction factor in cytokine production, by both the immune system and skeletal muscle,(18) and the profile of the produced cytokines depends on the type of exercise as well as its intensity and duration (10).

However, very few studies verify the profile of cytokines during and after resistance exercises. Brenner et al. (1999)(3) verified immune alterations and changes in the profile of cytokines IL-6, IL-10, and TNF-( under four different experimental conditions: control (5 hours seated), 5 minutes in bicycle ergometry (at 90% VO2max.), 2 hours in bicycle ergometry (at 60-65% VO2max.), and a session of circuit resistance exercise, consisting of five stations and completed in 3 series of 10 repetitions with 60-70% of 1-RM in each station. Significant increases were not found in the cytokine plasmatic levels under all the experimental conditions, except for the prolonged exercise (2 hours of bicycle ergometry).

There have been considerable increases found in plasmatic cytokines after exhaustive exercise such as a marathon,(12) a triathlon,(13) and cycling competitions,(6) all of which have durations superior to one hour and are of competitive intensity. Resistance exercises have also been demonstrated to alter the profile of cytokines generating muscle damage; however, these were exercises that exclusively gave priority to the eccentric phase of the movement.(1, 9). While the immune response to aerobic training has received great attention, much less is known about the acute changes in circulating cytokines induced by a single resistance training session or following a number of training sessions (16).

The objective of this study is, then, to evaluate the effect of a circuit resistance training program on the acute action of two fatigue tests (a bench press and a 45˚ leg press) on the levels of plasmatic cytokines including interleukin 8 (IL-8), interleukin 10 (IL-10), interleukin 6 (IL-6), interleukin 1β (IL-1β), and tumour necrosis factor ( (TNF-().

METHODS

Subjects

In total, 14 sedentary women participated in this study (they had not been practicing any regular physical activity for at least one year), with average age 39.8 ± 3.9, weight 57.8 ± 7.8 kg, and height 163.6 ± 6.6 cm. All of them were submitted to a previous clinical evaluation, and they were considered healthy, non-smoking, and having a normal menstrual cycle. The volunteers were informed about the possible risks of the study. They all promised not to use any medicine during the training. They also signed a consent term that was approved, along with the project of this research, by the Committee of Ethics and Research of The University of São Carlos.

Procedures

Fatigue tests and One Repetition Maximum (1-RM) were done with the 45( leg press and the bench press exercises. Lean body mass evaluation was done before and after the period of intervention, which consisted of 10 weeks of circuit resistance training. In order to analyse the profile of cytokines, blood collections were done before and after the fatigue tests. Each volunteer had her time of evaluation and training determined before the beginning of the evaluations. This procedure allowed the evaluations and training to always be conducted at the same time for each subject until the end of the research. The volunteers were instructs not to perform any type of exercise during the period of research.

Tests of 1-RM were done on the same day, with intervals of 20 minutes and random order of test completion. The procedures used for warm-up were to perform three series. The first set of 20 reps with the weight`s machine, the second set of 10 repetitions with ~ 50% of estimated 1-RM and the third set of 3 reps with ~ 70% of estimated 1-RM with an interval of one minute. The procedures adopted for warm-up and testing are in accordance with the review by Brown & Weir (2001)(4). A week before the test, the volunteers performed a familiarization session with the equipment and procedures adopted. The test consisted of a maximum of five attempts with intervals of three minutes, with the load added to each attempt. The movement started by the eccentric phase. All the subjects were able to obtain their 1-RM within the five attempts, with an average ± standard deviation of 3.9 ± 0.7 attempts. The volunteers were oriented to do the movements at their complete amplitude. When this procedure was not obeyed, the attempt was considered invalid. Additionally, all volunteers received a verbal stimulus by the same evaluator.

The fatigue tests were also done with two distinct exercises, with an interval of 48 h and their order defined by drawing. The tests consisted of three series separated by one-minute intervals, with intensities at 50% of 1-RM, and the volunteers were instructed to do the maximum number of repetitions until movement concentric failure occurred. Before the completion of the fatigue tests, the subjects did a standard warm-up with a series of 20 repetitions with weights (leg press equipment at 26 kg and bench press equipment at 9 kg). The volunteers were oriented to do the movements at their complete amplitude. When the procedure was not obeyed the repetition was not included. The time of movement was standardised at 1.5 s for the eccentric phase and 1.5 s for the concentric phase. However, the test was not interrupted if time was not adhered to during the last repetition of each series. In the leg press the subjects were placed with feet shoulder-width apart and were instructed to keep their feet on the platform fully supported throughout the execution of the movement. In bench press the grip widths was set with the bar resting on the chest and the elbow presenting an angle of 90 degrees.

Lean Body Mass (LBM) was analysed through DXA (Dual-energy X-ray Absorptiometry) with the LUNAR® trend, model DPX Plus # 6243, USA, Software version 4.7, with a variation coefficient in vivo of 0.9-1.1%, in a dorsal decubitus position, before and after the training period. Muscular endurance was determined through the number of repetitions done in the first series of fatigue tests, completed before and after training.(5)

In order to analyse the cytokines for the fatigue tests, the volunteers were divided through draft into 2 groups of 7, a 45( leg press group and a bench press group. However, it was not possible to perform venipuncture on two volunteers after the tests, so the groups constituted of six subjects. Before and after the fatigue tests, pre and one week post-training, samples of 5 mL of blood were collected from the antecubital vein and placed in a glass tube (Vacutainer), with the volunteers seated. The tube was kept in ice until centrifugation in 2,500 rpm at 4ºC for 20 min. Plasma was separated from the cells and stored at -80(C for subsequent analysis of the cytokines IL-8, IL-10, IL-6, IL-1(, and TNF-(, by flow cytometry (BD FACS Canto-Flow Cytometer – USA).

During the fatigue tests, 25 μl of blood was collected from the ear lobe into capillary tubes containing heparin, at the following moments: resting (REST), immediately after the first (AS1), second (AS2), and third (AS3) series of fatigue tests, and 5 min after the test (5 mA). Samples were kept in eppendorf-type tubes containing 50 (l of sodium fluoride and kept in a freezer at -20(C for further analysis in a lactate analyser (YELLOW SPRINGS 1500, EUA).

The lactate index for lean body mass was obtained by dividing the lactate blood concentration (mmol/L) of the fatigue tests by the lean body mass, for both the 45( leg press and the bench press. It represents the lactic anaerobic contribution related to the lean body mass in fatigue tests before and after training.

The volunteers completed a circuit resistance training of low repetitions for a period of 10 weeks, 3 times a week. Two turns in a circuit were completed in each training session, except the first had only one turn for training adaptation. The circuit consisted of 9 exercises in the following order: smith-machine squat, wide-grip pulldown to front, bench press with the guided bar, leg press at 45(, one-arm dumbbell row (starting with the non-dominant member), incline dumbbell press, leg curl, wide-grip upright row, and crunch curl. The interval between each exercise and between the circuit returns was standardised at one minute. The training load was determined between 8 and 12 repetitions maximum (RM). Before the beginning, two rounds in the circuit were completed for the adjustment of loads in the first training session. At the beginning of each session, a standard warm-up was done. All trainings were supervised by a personal trainer in order to correct wrong positions and adjust loads. Increasing load was done when the volunteers performed more than 12 repetitions in a series for any of the exercises.

Statistical Analyses

Normality tests (Shapiro Wilkes) were applied to all variables. When abnormal distributions were detected, were applied with the Wilcoxon Matched Pairs Test. When normal distributions were detected before and after training, the Test t Student was applied for dependent samples. For both tests, the adopted significance level was p < 0.05. With the sample size used (N = 6) for paired observations, the study has a power of 25.5% for analysis of cytokines. For statistical analysis, the Statistics program version 6.0, USA was used.

RESULTS

Except for IL-8, cytokines analysed before and after fatigue tests did not reach their limit of detection in plasma, both for the 45( leg press and the bench press, before and after training. (Table 1). Significant increases were found in the 1-RM for the leg press at 45( and the bench press, at 18.57% and 15.27%, respectively (Fig. 1A). The leg press at 45( exercise presented a significant decrease in

muscular endurance, with pre-training at 42.14 ± 9 repetitions and post-training at 35.36 ± 8.6 repetitions.

For the bench press exercise, significant differences were not found, with pre-training at 24.71 ± 7.92 repetitions and post-training at 28.21 ± 7.61 repetitions (Fig. 1B).

LBM increased significantly from the pre-training period 35.93 ± 4.93 kg to the post-training period 39.13 ± 4.95 kg (Table 2; Fig. 2A).

The lactate/LBM index decreased significantly for the 45( leg press at REST, AS1 and AS2, and for the bench press at REST, AS1, AS2, AS3 and 5mA, when pre- and post-training periods were compared (Fig. 2B).

DISCUSSION

We did not find significant alterations in the cytokine profile after two fatigue tests when related to pre-exercise values. Besides that, modifications in cytokines were not verified after 10 weeks of circuit resistance training. However, the training notably provoked alterations, such as lean body mass increases, strength increases and lower concentrations of lactate in fatigue tests, showing that gains in neuromuscular and metabolic fitness do not have a relationship with the profile of cytokines analyzed in this study.

The Nature of the Stimuli and Cytokine

The non-alteration in the profile of cytokines found in our study is in accordance with Brenner et al. (1999),(3) which did not find alterations in the plasmatic concentrations of IL-6, IL-10, and TNF-( after a session of circuit resistance exercises with 60-70% of 1-RM and duration of 45 min. These results, however, are in discordance with Anwar et al. (1997),(1) which accomplished 4 series of 10 repetitions with 100% of 1-RM in an eccentric press exercise (leg) and found plasmatic increases of IL-6 with subsequent reduction of IL-1. Paulsen et al. (2005),(14) after 300 maximum eccentric actions in an isokinetic apparatus with quadriceps muscle, did not find alterations for IL-8. Nonetheless, they observed increases of IL-6 immediately after the exercise. However, a correlation between the amount of work completed and the concentration of cytokines was not found in this study.

When comparing aerobic exercises with eccentric ones, it has been demonstrated that the biggest changes in plasmatic cytokines occur in endurance exercises. For this reason, there could be other factors, beyond muscle damages, involved in the cytokines alterations in blood in the case of aerobic exercises. This difference could be due to the fact that eccentric exercises induce few energetic oxidative and metabolic stresses (besides a small hormone alteration), which are stimuli known for the liberation of systemic cytokines.(15)

In this way, the nature of the stimuli seems to be primordial in the response profile of cytokines produced after the exercise. High intensity eccentric exercises have been demonstrated to alter the profile of cytokines through the generation of muscle damage.(14, 1) Despite that, our model of exercise (fatigue tests), which also has a big eccentric component, did not present such responses. This could be due to the low load used (50% 1-RM) or even to some eventual effect of the completion of the concentric phase of the movement. However, this work was dedicated to analysing the response of cytokines to dynamic resistance exercises realising both phases of movement, i.e. the concentric and eccentric ones.

Chronic Adaptations

After the training period, we found increases in the 1-RM of the two exercises evaluated (leg press at 45( and bench press), which also provoked increases in the load of completion for the fatigue tests. This allowed a reduction in the muscular endurance for the leg press at 45( and maintenance for the bench press, probably due to the characteristic of training, which emphasized the more strength gains than resistance. As has been previously reported (Izquierdo et al. 2009) (8), after a short-term strength training period, when the relative intensity of the fatiguing dynamic protocol was kept the same, the magnitude of exercise-induced loss of functional capacity was greater than that observed before training, but lower fatigue occurred when the same absolute load was used. However, data indicate that the training was efficient to augment the maximum dynamic force and the absolute muscle endurance in the fatigue tests. Additionally, the lactate/LBM indices were significantly smaller during REST, AS1, and AS2 for the leg press at 45(, and during REST, AS1, AS2, AS3, and 5 mP for the bench press, which indicate metabolic alterations of the fatigue tests over the 10 weeks of training.

Baum et al. (1999)(2) found increases in the synthesis of IL-1( and IL-6, after 12 weeks of running training with a duration of 3-5 hrs per week. As previously demonstrated, our results did not agree; this is possibly due to the completion of resistance training for strength gain and not for aerobic capacity, indicating that the nature of the exercise plays an important role in the cytokine response to training and that neuromuscular and metabolic adaptations do not have a relationship with the cytokine profile after resistance exercise.

Resistance exercise and Inflammation Systemic Biomarkers

A study conducted with individuals separated into four groups (inactive youngsters, active youngsters, inactive old individuals, and active old individuals) did not find alterations in the biomarkers of inflammation after 12 weeks of combined aerobic and resistance training, except for a significant reduction in the levels of CRP.(19) White et al. (2006)(21) found alterations in these markers after 8 weeks of resistance training in individuals with multiple sclerosis. Prestes et al. (2009) performed a resistance training for 16 weeks in elderly sedentary and found reductions in the levels of IL-6 after training (17).

This study did not identify resting alterations in the inflammation systemic biomarkers, which could indicate that circuit resistance exercise is efficient to promote positive adaptations to health without compromising inflammation biomarkers. However, the short period of training and the differences among the populations studied can explain the different results, with it easier to find alterations in sick populations during a period of 8-12 weeks of training.(21)

Physical exercise has been defended as a prototype of the physical stress like many clinical physical stressors (e.g. surgery, trauma, burnt, sepsis), which induce standards of hormone and immunologic response similar to those of the exercise.(15, 7) Local and systemic reactions to infections and muscle damage depend in part on the magnitude of the cytokine response.(17) The non-detection of pro-inflammatory (IL-1( and TNF-(), anti-inflammatory (IL-10), responsive to inflammation (IL-6), and chemio-attractive cytokines (IL-8) in both exercises (leg press at 45( and bench press) led us to believe that dynamic resistance exercises completed until exhaustion do not alter the immunologic response, since they do not provoke alterations in the cytokine profile. (11)

CONCLUSIONS

Resistance exercises of three series, separated by 1-min intervals and completed until exhaustion, did not alter the profile of plasmatic cytokines before or after 10 weeks of in-circuit resistance training. However, the training provoked neuromuscular and metabolic adaptations. Our data, then, support the idea that the two fatigue tests done do not provoke stress sufficient to alter the plasma concentrations of IL-6, IL-8, IL-10, IL-1β, and TNF(, in this way, they cannot be considered as a prototype of physical stress.

ACKNOWLEDGEMENTS

National Counsel of Technological and Scientific Development (CNPq) for the scholarship in the development of this work.

Address for correspondence: Nunes JED Ms., Benjamin Constant Street, 1286, Aparecida, Postal/zip code: 38400-678, Federal University of Uberlândia – Laboratory of the Physiology of Performance, Uberlândia, Minas Gerais, Brazil. Phone (34)3218-2963; FAX: (34)3218-2910; Email. joaoelias@faefi.ufu.br

REFERENCES

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Journal of Exercise Physiologyonline

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Volume 13 Number 3 June 2010

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Table 1. Concentration of cytokines before and after the completion of a fatigue test (FT) on the bench press and on the Leg Press 45(.

| |Bench Press |Leg Press 45( |

| |Pre-T (pg/ml) |Post-T(pg/ml) |Pre-T (pg/ml) |Post-T (pg/ml) |

|Cytokines |BFT |AFT |BFT |

|Body Weight (kg) |57.7±7.8 |56.9±6.3 |0.370 |

|BMI (kg/m2) |22.6±1.6 |22.7±1.6 |0.766 |

|FM (kg) |21.9±8.1 |17.8±4.2 |0,021 |

|LBM (kg) |35.9±4.9 |39.1±4.9 |0.000 |

Values represent mean ± SD. Abbreviations: BMI; body mass index, FM; fat mass, LBM; lean body mass.

Figure 2 – A: Lean Body Mass (LBM), pre and post-training. *Post x Pre (p < 0,01). B: Lactate/LBM pre and post-training. Leg Press 45˚ (LP) and Bench Press (BP). Rest, After Series 1 (AS1), After Series 2 (AS2), After Series 3 (AS3), and 5 minutes after (5mA) the fatigue test. *Post x Pre LP (p < 0,01), +Post x Pre BP (p < 0,05).

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